The Dentition

Chapter 21

The Dentition: Development, Disturbances, Disease, Diet, and Chemistry Rebecca Kinaston1, Anna Willis2, Justyna J. Miszkiewicz3, Monica Tromp1,4 and Marc F. Oxenham3 1

Department of Anatomy, School of Biomedical Sciences, University of Otago, Dunedin, New Zealand, 2College of Arts, Society & Education, James

Cook University, Townsville, QLD, Australia, 3School of Archaeology & Anthropology, Australian National University, Canberra, ACT, Australia, 4

Department of Archaeology, Max Planck Institute for the Science of Human History, Jena, Germany

INTRODUCTION This chapter is concerned primarily with the dentition, with brief discussions of associated structures such as supporting alveolar bone, where relevant. Dental development, including the dentin and enamel, is reviewed in the first section. This is followed by a discussion of disturbances in the dentin and enamel in the second section. The third section looks at the identification of oral disease, including caries, alveolar lesions, antemortem tooth loss (AMTL), and periodontal disease. This is followed by the fourth section, which focuses on interpreting oral health, particularly in the context of sex differences and major demographic transitions. The fifth explores dental chemistry in terms of paleodietary reconstruction, breastfeeding and weaning, stress and disease, and finally mobility and migration. The final section discusses dental calculus in the context of microparticle and then chemical analyses of calculus. Ancient DNA (aDNA) and protein analyses of dental calculus are also reviewed.

DENTAL DEVELOPMENT Due to their high mineralization content, teeth preserve very well in the archeological record. Unlike bone, dental tissues are not considered predominantly “dynamic,” i.e., tissues that continuously remodel or adapt to external and internal stimuli. However, they follow a timed and sensitive process of tissue development and formation, and thus serve as a long-lasting record of growth and potential physiological disruption a once-living individual would have experienced. Enamel and dentin are frequently

studied in paleopathology (Beaumont et al., 2013b; Goodman and Rose, 1990; Reid and Dean, 2000, 2006; Sandberg et al., 2014), and are the focus of the first section of this chapter.

Dentin Dentin, along with enamel, forms “true” teeth in all vertebrates (Hall, 2015). It lies directly underneath enamel, and is primarily composed of B70% inorganic material, B20% organic, and B10% water (Nanci, 2012). Dentin formation is executed by odontoblast cells, which combine sialoprotein and phosphoprotein to secrete, synthesize, and mineralize dentin (Gopinathan et al., 2013). Odontoblasts are also mechanosensitive and immunedefensive cells, which means that dentin has reparative capabilities (Couve et al., 2013; Goldberg et al., 2011), and they originate in neural crest cells (Gopinathan et al., 2013). As the tooth crown forms, they lay down dentin as the first mineralized tissue, which next induces the production of enamel (Nanci, 2012). However, the differentiation of odontoblasts requires precursor enamel cells, meaning that there is a “reciprocal induction” between enamel and dentin (Guatelli-Steinberg and Huffman, 2011: 98). This begins in the cusp and extends down the forming tooth. The resorption of root dentin is undertaken by odontoclasts (Sasaki, 2003). Dentin is initially deposited in the form of predentin (primarily composed of glycosaminoglycans and type I collagen), and secondly mineralized by hydroxyapatite. Key genes involved in dentin development, and determining dentin mineralization, are Runx2, Msx2, COL1A1/COL1A2, SIBLINGs, and

Ortner’s Identification of Pathological Conditions in Human Skeletal Remains. DOI: https://doi.org/10.1016/B978-0-12-809738-0.00021-1 © 2019 Elsevier Inc. All rights reserved.

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DSPP (Gopinathan et al., 2013; Hart and Hart, 2007; Rajpar et al., 2002). Dentinogenesis is a tightly controlled process of dentin development and formation. The differentiation of odontoblasts commences during the crown formation phase in developing teeth (2nd trimester in utero in deciduous incisors), and once mature they occupy the pulp cavity to begin the secretion of unmineralized predentin (Nanci, 2012). The predentin zone is approximately 10 40 μm (Hart and Hart, 2007). Type I collagen secreted by odontoblasts is deposited into this zone and collagen fibril structuring begins. This phase is accompanied by a release of ions and proteins which induce the formation of apatite. As odontoblasts secrete the organic matter, they elongate and leave extended odontoblast processes behind. Once mineralized, the matrix becomes mantle dentin, which measures approximately B150 μm (Hart and Hart, 2007). Based on the formation stage, dentin can be categorized into primary, secondary, and tertiary (Guatelli-Steinberg and Huffman, 2011). Primary dentin is associated with a smaller amount of deposited collagen, which is also more tightly organized into fibrils, and is laid down during crown and root formation. Secondary dentin takes longer to form, occurs once root formation is completed, and is not unfirmly distributed across the tooth. Tertiary, or reparative, dentin forms in response to disturbances that may include caries or other abnormal stimuli (Hart and Hart, 2007). The structure of dentin is hierarchical in its organization (Kinney et al., 2003). The inorganic crystals are nanocrystalline apatite, needle- and plate-like shaped, approximately 5 nm thick. The type I collagen fibrils range between 50 and 100 nm in diameter. Their orientation is random, but perpendicular to the direction of dentin formation. The mineral component within the collagen is both intra- and extrafibrillar (inside and outside of the fibrils) (Kinney et al., 2003). The microstructural appearance of dentin is fiber or tubular like, shaped in cylindrical units. These extend from the dentin enamel junction (DEJ) to the root pulp. Each tubule is B3 μm thick near the pulp, and B0.06 μm thick near the DEJ (Linde and Goldberg, 1993). These dentin tubules essentially indicate paths created by odontoblasts, and these are also where the odontoblast processes, along with liquid matter and proteins, are found (Guatelli-Steinberg and Huffman, 2011). Dentin can be inter- or intratubular (formed outside or inside the tubules), and its curvature ranges from S-shaped to straight in the crown and the root, respectively (Nanci, 2012). This dentin architecture equips it with a range of tissue strength and fracturing properties depending on the level of mineralization. The elasticity (Young’s modulus) of dentin has been suggested to range between 20 and 25 GPa, and it withstands (beyond

mastication stress) an approximate 30 MPa of load before it fatigues (Kinney et al., 2003). Dentin growth is incremental (Dean, 2000). In histological thin sections, viewed using light microscopy, dentin microstructure can be subdivided into short- and long-period incremental lines, both of which are thought to represent a biological growth rhythm of an organism (Dean and Scandrett, 1996). The short-period lines form daily, and are known as von Ebner’s lines; whereas the long-period lines take up to several days to form, and are known as Andersen lines (Dean, 2000). von Ebner’s lines are approximately 2 5 μm, whereas Andersen lines are spaced 15 30 μm apart (Dean et al., 1993). The periodicity of Andersen lines corresponds to the increments in enamel, ranging between 6 and 12 days (Dean, 1987; Dean et al., 1993). Dentin incremental structure, and its underlying daily or longer rhythm of growth, has served as a tool for reconstructing dental growth and life history in several animals (e.g., Erickson, 1996a,b), but its implications for paleopathology remain less studied than enamel in human tissue (Dean, 2000). For example, the use of dentin increments in human tooth development research has identified long-term administration of tetracycline antibiotics in one case study (Dean et al., 1993), and differences in short-duration nutritional abnormalities from stable isotope data retained within dentin increments (Beaumont et al., 2013b; van der Sluis et al., 2016). Dentin microscopic lines can also be used to reconstruct age-at-death from teeth with incomplete roots but formed crowns, by combining crown formation rate (calculated from enamel) and estimated root extension growth rate (Dean and Vesey, 2008; Macchiarelli et al., 2006). Finally, in paleopathological contexts, dentin examination is routinely undertaken in dental wear age-at-death estimation methods, and dentin lesions associated with caries or other oral bacteria (see “Identifying Dental Wear and Oral Disease” section). It is becoming clear that microstructural investigation of dentin structure has the potential to assist with the reconstruction of tooth growth (Guatelli-Steinberg and Huffman, 2011), though as Hillson (2005) notes, its daily increments are not always clearly identifiable in sections.

Enamel Enamel envelopes the underlying dentin and is the most outer layer of dental crowns. It is the most highly mineralized and avascular tissue in all vertebrates (Hall, 2015). When compared to dentin and bone, which derive from mesenchyme, enamel is the only extracellular skeletal tissue with an epithelial origin (Soukup et al., 2008). Its extracellular matter does not contain collagen, rather it is composed of enamelin and amelogenin proteins

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(Doi et al., 1984). Enamel is almost completely mineralized, with approximately 96% inorganic (hydroxyapatite) and 4% organic and liquid components. It is formed by ameloblast cells which originate in ectodermal epithelia (Miletich and Sharpe, 2003). Key proteins involved in the formation of enamel are amelogenin, enamelin, ameloblastin, tuftelin, matrix metalloprotein-20, and serine proteinase (Brookes et al., 1995; Guo et al., 2015; Hall, 2015). Amelogenin is the most abundant, while enamelin is the largest and the least abundant (Al-Hashimi et al., 2009; Brookes et al., 1995). The process of enamel development and formation is known as amelogenesis, which begins by a deposition of the organic matter to be later mineralized by hydroxyapatite (Bronckers, 2017). Amelogenesis commences in the second trimester in utero, when deciduous incisors begin calcification (Kraus and Jordan, 1965; Nanci, 2012). Enamel in all deciduous teeth undergoes calcification in utero, with only the first permanent molar forming before or around the time of birth (Lunt and Law, 1974; Mahoney, 2011). As enamel matures over the prenatal, child, and teenage years of life, its structure retains normal growth and disruption information (Hillson, 2005). Unlike dentin, enamel is acellular and does not continue to form once tooth crown growth is completed. It begins development during crown tip formation, when ameloblast differentiation, preceded by odontogenesis (as earlier), initiates secretion of enamel proteins (Nanci, 2012). As the organic matrix is produced, cell differentiation continues along the DEJ until mature ameloblasts are able to move away in the direction of the future enamel surface (Simmer and Fincham, 1995; Simmer and Hu, 2001). At the same time, dentin undergoes mineralization, and ameloblasts join with mantle dentin collagen fibrils (Hu et al., 2007). Unlike bone or dentin (osteoid and predentin, respectively), there is no “preenamel” matter formed, but the secreted enamel simply occupies a mineralization zone. As this zone recedes, ameloblasts develop Tomes’ processes, which are secretory protrusions involved in the lengthening of enamel crystals (Franklin et al., 1991). Enamel matrix is deposited on the surface of dentin, enlarges and grows until the initial, aprismatic enamel layer is formed (Hu et al., 2007). This is the secretory stage of formation, where enamel produced is approximately 30% mineralized (Guatelli-Steinberg and Huffman, 2011). Tomes’ processes shape the organization of enamel crystals into rod and inter-rod structures (Habelitz et al., 2001). The rods, or prisms, are aligned perpendicular from the DEJ to tooth surface, and are composed of carbonated hydroxyapatite, enamelin-coated crystals which are positioned along the rod axis (Jeng et al., 2011). They measure approximately 4 5 μm in thickness (Huang et al., 2010). The inter-rod enamel are the spaces between rods, which are protein-rich and

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approximately B1 μm thick (Huang et al., 2010). The hierarchical organization of enamel, and the composite orientation of enamel apatite crystals, give enamel anisotropic mechanical properties which determine dental stress dissipation and fracturing properties (Habelitz et al., 2001). The elasticity of a single enamel rod has been noted to range between B87.5 and 72.7 GPa on the Young’s modulus scale, whereas its approximate hardness ranges from B3.9 to 3.3 GPa (Habelitz et al., 2001; Huang et al., 2010). At the histological level, similarly to dentin, enamel presents with a series of incremental lines that reflect its rhythmic and timed deposition (Reid and Ferrell, 2006). Just like in dentin, enamel increments can be divided into daily markings (short-period cross-striations), and longerperiod lines known as Retzius lines or striae of Retzius (Dean, 2000). The daily cross-striations are spaced every 4 μm and lie in between the thicker and darker Retzius lines. These striae of Retzius manifest as perikymata on the outer tooth surface, seen as a series of horizontal lines or bands. Unless worn, they can be observed on the lateral surfaces of outer enamel, but they remain “buried” in cuspal enamel (Guatelli-Steinberg and Huffman, 2011: 94). Retzius lines form when enamel matrix secretion slows down systemically, which happens at regular increments in all forming teeth (Dean, 1987). It is therefore possible to calculate Retzius periodicity by counting the number of daily markings between adjacent Retzius lines, which seems to average between 6 and 12 days in humans (Reid and Dean, 2006). This incremental premise of enamel formation has been used to create standards for reconstructing dental formation times in human and nonhuman primate teeth (Reid and Dean, 2000, 2006; Reid and Guatelli-Steinberg, 2017; Smith et al., 2007, 2010), whereby perikymata, Retzius periodicity, and crown height can be combined to estimate crown formation times. In paleopathology, these standards of enamel increments have mainly been applied when determining the timing of enamel disturbances. Enamel markings and their periodicity have been studied over the past two centuries, revealing their value in dental growth research (Boyde, 1963; Dean and Scandrett, 1996; Retzius, 1837). Several studies utilizing larger and smaller bodied animal teeth (e.g., mammoths, monkeys) identified a link between body size and Retzius periodicity (e.g., Fukuhara, 1959; Koch and Fisher, 1986), and a circadian nature of cross-striation periodicity (e.g., Hogg et al., 2015; Massler and Schour, 1946), indicating that a centralized biorhythm may be coordinating the deposition of skeletal tissues (see Antoine et al., 2009; Bromage et al., 2009, 2012). Its nature remains enigmatic for humans, as it seems to vary intraspecifically (Mahoney et al., 2016). As our understanding of skeletal biorhythms unfolds, it will no doubt have vast implications for the study of ancient human remains.

752 Ortner’s Identification of Pathological Conditions in Human Skeletal Remains

Another type of darker striae seen histologically is the neonatal line which forms at the time of birth, and indicates an intersection between pre- and postnatal enamel (Weber and Eisenmann, 1971). Identifying its presence from dental thin sections has allowed paleopathologists to study prenatal or childhood mortality, morbidity, and development (e.g., Kurek et al., 2016; Miszkiewicz and ˙ ˛dzi´nska et al., 2015). By locating the Mahoney, 2017; Za neonatal line, and counting daily markings, the incremental structure of enamel can also help paleopathologists estimate a child’s age-at-death from dental crown remains that had not completed formation before death (Boyde, 1963, 1990; Mahoney, 2011; Smith et al., 2006).

DISTURBANCES IN DENTAL DEVELOPMENT Abnormal Quality of Teeth: Disturbance of Dentin Development Pathology Disturbances in dentin development can be inherited or acquired. The former can be broadly categorized into dentinogenesis imperfecta (DI) and dentin dysplasias (DD) (Hart and Hart, 2007; Shields et al., 1973). These are usually inherited via autosomal dominant pathways, and have been documented in a variety of different syndromes, including: osteogenesis imperfecta, rickets, and other conditions associated with abnormal calcium deposition (see Chapters 16 and 19; Hart and Hart, 2007). In DI, human teeth (both deciduous and permanent) exhibit these abnormalities usually in the form of tooth discoloration (e.g., different shades of brown), weak and fracture-susceptible enamel, and bulging tooth crowns with abnormally small roots and pulp cavities. At the histological level, dentin tubules appear irregular and are absent in some areas. This condition causes enamel to shatter easily and accrue wear at a faster rate. DI can be subdivided into types I, II, and III (Hart and Hart, 2007). Type I DI is due to a mutation in the COL1A1/COL1A2 gene (Pollitt et al., 2006), and is associated with osteogenesis imperfecta. Thus, individuals with an unusually high rate of dental wear for their age ought to also be examined for postcranial trauma, joint abnormalities, and stature. Type II DI is associated with a lack of other, nondental lesions and/or symptoms. Type III DI (gene DSPP) presents with crown discoloration and enlarged pulp chambers, and pitting in enamel. DD are not associated with tooth discoloration, but are diagnosed mainly by obliterations in the pulp cavity caused by defective dentin. This type of defect is subdivided into types I and II (Brenneise and Conway, 1999; Kalk et al., 1998). In type I DD permanent and deciduous

dental crowns exhibit no abnormalities, but roots are shortened and mobile, which leads to premature breakdown. In type II DD, only the deciduous teeth show features of type II DI, and are additionally associated with pulp stones. No root changes, as seen in type I DD, are observed. Disturbances to dentin growth that are acquired usually include some form of abnormal stimuli, such as attrition or carious lesions. Unlike enamel, dentin is cellular and thus responds to these stimuli by producing tertiary dentin, which is also known as “reparative” (Hart and Hart, 2007; Klinge, 2001). Tertiary dentin appears irregularly structured and is usually found in locations where external irritation would have occurred (Ricucci et al., 2017). Tertiary dentin has been observed in older and slower-developing carious lesions, but absent in rapidly developing ones (Bjørndal, 2001). It has been reported in primary teeth from individuals with vitamin D-resistant rickets (Hillmann and Geurtsen, 1996), or those suffering from dental injuries (Robertson, 1997). At the histological level, disturbances to the incremental growth of dentin can be deduced from the presence of accentuated markings known as Owen’s lines or contour lines of Owen (Dean, 2000). These are not incremental because they occur irregularly and are thought to form in response to illness or environmental upsets (Dean et al., 1993). Their etiology remains unclear, but it is most likely that they accentuate following a disruption to calcium metabolism, and thus simply present as thickened or darkened lines, similar to the neonatal line in enamel (Schour and Hoffman, 1939). They also seem to correspond to accentuated lines in enamel, both of which meet at the DEJ, though not in the exact same location given that dentin precedes enamel formation (Guatelli-Steinberg and Huffman, 2011).

Paleopathology Owen’s lines indicating disturbances to the incremental growth of dentin have been previously reported in dentin from modern humans with conditions such as cleidocranial dysostosis (Fukuhara, 1959), but remain rarely reported in paleopathology. The few studies examining these lines in archeological samples have linked their occurrence to disturbances in enamel to gain a more comprehensive understanding, encompassing more than one type of dental tissue, of systemic health disruptions (see discussion of enamel hypoplasia (EH) below). For example, Witzel et al. (2008) matched Owen’s lines to disturbances captured by enamel in tooth sections representing humans from an early medieval site (5 7th centuries AD) in Barbing, Germany. Out of a total of seven teeth analyzed microscopically, one canine specimen exhibited an Owen’s contour line in association with its enamel

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equivalent. This specimen demonstrated, health disturbance at the dentinogenesis stage, which would not have been otherwise inferred from macroscopic analyses of the teeth alone. Future studies may, therefore, benefit from investigating dentin at the microstructural level (Dean, 2017), as inherent skeletal pathology may lead to defective dentin, which in turn may underlie one’s susceptibility to accumulating caries or rate of dental wear.

Abnormal Quality of Teeth: Disturbance of Enamel Development Pathology Disturbances to the process of amelogenesis, and more specifically enamel secretion by ameloblasts, lead to a variety of defects in the final quality (mineral) or quantity of enamel, including thinning, hypoplastic changes, and hypermineralization (Hu et al., 2007). These can be inherited, usually as a result of abnormal proteins involved in mineral metabolism (e.g., abnormalities associated with parathyroid gland function). In this case, if abnormal enamel only originates in the dentition, the defects are known as amelogenesis imperfecta (Witkop, 1988). However, defective enamel can also develop due to other systemic conditions associated with altered skeletal mineralization pathways. Amelogenesis imperfecta manifests in three different ways (Hu et al., 2007). It can be associated with an abnormally thin (hypoplastic) layer of enamel (in extreme cases there may be hardly any enamel present on the tooth). Enamel may become hypomineralized (lack of, or poor, mineralization), where its thickness is unaffected but extreme softness increases the rate of wear and calculus accumulation. Enamel can also undergo hypomaturation, which manifests by way of discolored (brown to yellow) crowns with dentin-like tissue density. Acquired enamel defects form when severe enough physiological/systemic or environmental disturbance disrupts the highly sensitive and incremental enamel development. This results in localized areas of hypoplastic enamel, which manifest macroscopically on the outer tooth surface as “depressed” perikymata. They are categorized broadly as EH, a “marker” of childhood physiological health disruption. The literature suggests a variety of factors underlying the formation of EH, including systemic (e.g., malnutrition, illness, weaning), or localized (e.g., trauma) stimuli, exposure to toxins and radiation, environmental upsets, as well as epigenetic effects (such as DNA methylation) (Boldsen, 2007; Geber, 2014; Sarnat and Schour, 1941; Seow, 2014). Therefore, EH is considered a nonspecific dental lesion. The macroscopic expression of EH can take many forms, such as grooves, irregular pits, or furrows (Hillson,

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2005). At the histological level, enamel development disruption is recorded in the form of accentuated lines, sometimes referred to as Wilson bands (FitzGerald and Saunders, 2005). These are similar in appearance to Retzius lines, except they are darker and thicker (Goodman and Rose, 1990; Witzel et al., 2008). By studying these accentuated markings, it is possible to reconstruct the age at which a stressful event would have taken place (by referring to standards for tooth formation times, e.g., Reid and Dean, 2000), which may not be otherwise possible if, for example, the outer tooth surface presents with invisible perikymata (Cares Henriquez and Oxenham, 2017; Hassett, 2012). Studies have shown a link between the accentuated markings and their macroscopic expression (e.g., Witzel et al., 2008), though a microscopic approach linking enamel and dentin disturbances is argued to offer a fuller picture of stress affecting dental development. EH may not form on all the teeth that are developing during the period of systemic stress. Furrow, or linear enamel hypoplasia (LEH), presents as horizontal bands of depression that run along the outer tooth surface. It has been observed that the anterior teeth (incisors and canines) display a higher prevalence of LEH than posterior teeth and this is thought to be a result of the strong genetic control over the formation of the latter (Goodman and Armelagos, 1985). Canines take the longest period of time to form and are therefore potentially more susceptible to periods of stress than other teeth (Lewis, 2007). The presence of hypoplastic defects in the deciduous dentition can point to periods of stress during the third trimester in utero until about the age of 1 year (Goodman et al., 1987). Hypoplastic defects located on the deciduous dentition have also been observed as areas susceptible to caries development after birth (Cook and Buikstra, 1979; Hillson, 2008). The defective mineralization of the crown enamel as a result of these developmental defects is thought to predispose this area to the formation of circular caries (Larsen, 1997). A circular carious lesion is identified as a transverse carious band on the labial and/or buccal surface of the deciduous teeth (Cook and Buikstra, 1979; Cook, 1979). The presence of circular caries has been linked with stress during the prenatal and perinatal period, including diarrheal disease (Sweeney et al., 1971).

Palaeopathology Amelogenesis imperfecta is difficult to identify in archeological samples, but it can be considered as part of a differential diagnosis. EH assessments are routinely incorporated into paleopathological research (Armelagos et al., 2009; Guatelli-Steinberg and Lukacs, 1999; Hillson and

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Bond, 1997; Miszkiewicz, 2015; Ogden et al., 2007; Oxenham and Matsumura, 2008). Enamel hypoplastic defects are favored in paleopathology as indicating nonspecific “stress” in ancient populations (the definition of which is not agreed upon, see Reitsema and McIlvaine, 2014). However, LEH is most commonly observed and thus reported, and has been investigated in a plethora of studies in paleopathology (see Bocaege and Hillson, 2016; Ritzman et al., 2008). One example of nonlinear EH types, and its relationship to ancient human stress, is localized primary canine hypoplasia (LPCH). Out of 24 subadults from a Neolithic site of Man Bac in Vietnam (B4000 3500 BP), 41.7% were observed to display LPCH (McDonnell and Oxenham, 2014). Appearing as a rounded and localized depression on the labial deciduous canine surface, the defects can be linked to a series of nonspecific etiologies, including damage from object “mouthing” and nutritional upsets arising from vitamin A and D deficiencies. These can be extended to several interpretations and inferences about the potential stress experienced by mother and infants in this sample (Goodman and Rose, 1990). Given the relatively high prevalence of these defects, McDonnell and Oxenham (2014) suggest the presence of depressed maternal health at this site, which would agree with its transitionary stage into an agricultural subsistence economy. Alternatively (or complementarily), this could also be evidence for early childhood exploratory behaviors in ancient Man Bac. Linear enamel hypoplastic defects have been routinely documented in paleopathology, spanning many different time periods and geographical locations (e.g., Boldsen, 2007; Larsen, 1997; Miszkiewicz, 2015; Starling and Stock, 2007; Tomczyk et al., 2007). A series of ancient health and disease contexts have been studied using LEH data, including childhood disease and malnutrition (Goodman and Armelagos, 1988; Tomczyk et al., 2007), weaning (Blakey et al., 1994), socioeconomic stratification of ancient societies (Miszkiewicz, 2015; Nakayama, 2016), and mortality (Boldsen, 2007) to list a few. Tomczyk et al. (2007) found increased hypoplasia records on human teeth from archeological sites in the middle Euphrates representing humans who would have experienced food scarcity associated with historical periods of warfare, political violence, and economic crisis (late Bronze, early Neo-Assyrian, Roman, and Byzantine). Starling and Stock (2007) showed a gradual decrease in hypoplasia occurrence along with the development of the state in pastoralists from Nubia and Egypt. Miszkiewicz (2015) compared low- and highsocial status groups of late medieval humans in England, reporting lower age-at-death and higher LEH in the former group. This indicated poor childhood

health in children from lower-class backgrounds. Shorter longevity (i.e., lower age-at-death estimates) has been further associated with increased frequencies of LEH records in samples from medieval Denmark (Boldsen, 2007; Palubeckait˙e et al., 2002), Croatia ˇ (Slaus et al., 2002), and Lithuania (Palubeckait˙e et al., 2002). Weaning of children has also been previously discussed as potentially reflected in the age of LEH formation, particularly when estimated to have occurred between 2 and 4 years old (Blakey et al., 1994; Lanphear, 1990; Miszkiewicz, 2015). However, complementary lines of weaning age evidence are needed for these inferences to be convincing, given the variation in enamel formation times between populations (Reid and Dean, 2006), and the definition and practice of weaning in different cultures (Griffiths et al., 2007). Studying isotopic signatures linked to breast milk feeding from the increments in enamel may be a more reliable approach (King et al., 2017). Accentuated lines in enamel histological sections have not received as much attention in paleopathology as macroscopic evidence of LEH. However, in a study by Rose et al. (1978), Wilson bands studied at the microscopic level of enamel corresponded to increased mortality and abnormal skeletal lesions in samples from the Mississippian and Woodland archeological sites in the American Midwest representative of the maize agricultural transition. Traditionally, studies of LEH utilize the “field method,” whereby the outer tooth surface is visually examined, palpated, or viewed under small magnification for obviously depressed perikymata (see Brickley and McKinley, 2004; Hassett, 2012; Hillson, 2005). Formation times of the LEH can then be estimated from charts of tooth formation having divided the whole intact dental crown into age-associated sections. Reid and Dean’s (2000,2006) standards are particularly robust as they are based on enamel histological increments that account for appositional enamel (King et al., 2002). In recent years, studies have highlighted that a sole macroscopic approach does not account for all depressed perikymata, and thus potentially underestimates the frequency of LEH (e.g., Cares Henriquez and Oxenham, 2017; Hassett, 2014). Fig. 21.1 provides an example of an adult male individual from an archeological site in Fort Concho, Texas, United States (NMNH 243490), with evidence of multiple hypoplastic transverse lines on the canines. The upper incisors are missing and the lower incisors have been damaged postmortem. Figs. 21.2 and 21.3 are further examples of severe hypoplastic defects on the maxillary and mandibular dentition from a medieval individual from St. Gregory’s Priory collection at the University of Kent, Canterbury, UK (specimen NGA 88 SK 410).

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FIGURE 21.1 Multiple hypoplastic transverse defects of the canine teeth (adult male from Fort Concho, Texas, United States, NMNH 243490).

FIGURE 21.2 Anterior view of the left and right maxillary central incisor, right lateral incisor, and the right canine in a medieval individual (specimen NGA 88 SK 410) from St. Gregory’s Priory collection at the University of Kent (Canterbury, United Kingdom) displaying severe hypoplastic defects.

Abnormal Quality of Teeth: The Effects of Disease Pathology Infectious diseases, and metabolic and endocrine disorders experienced by an individual during the time of tooth development may cause malformation of the teeth (Kreshover, 1960; Nissanka-Jayasuriya et al., 2016; Pessoa and Galva˜o, 2011; Suckling et al., 1983; Sweeney et al., 1969). EH development is associated with environmental and physiological perturbations during tooth formation, and therefore any type of infection or disorder that may result in a period of systemic stress can act to disrupt odontogenesis and amelogenesis (Goodman, 1991, 1998). Important to note is the synergistic relationship

FIGURE 21.3 Lateral anterior view of mandibular dentition in a medieval individual from St. Gregory’s Priory collection (specimen NGA 88 SK 1222) at the University of Kent (Canterbury, United Kingdom) displaying less severe hypoplasia on the right canine and premolar. The perikymata depressions are shallower compared to NGA 88 SK 410 (see Fig. 21.2).

between undernutrition and infectious disease (Goodman and Rose, 1991), which is one reason why EH is considered evidence for nonspecific stress (Lewis and Roberts, 1997). Ortner (2003: 596) provides a few examples of individuals with likely or known diseases who had hypoplastic defects, which may have formed as a result of these conditions: a 6-year-old individual with suspected vitamin D deficiency (rickets) (Fig. 21.4) and two individuals (a 3- to 6-year-old child and a 17-year-old boy) with likely and confirmed tuberculosis, respectively (Figs. 21.5 and 21.6). Since the mid-19th century, it has been known that congenital syphilis (Treponema pallidum) interrupts tooth and enamel formation causing specific dental changes (reviewed in Ioannou et al., 2018). Methods to standardize these dental changes in the permanent dentition have led Hillson et al. (1998) to suggest four pathognomonic criteria to record: (1) Moon’s molars (an abnormally close

756 Ortner’s Identification of Pathological Conditions in Human Skeletal Remains

FIGURE 21.4 Dental hypoplasia associated with possible rickets. (A) Occlusal view of maxillary dentition; note defective crowns of second deciduous molars and right first permanent molar. (B) Occlusal view of mandibular dentition. The crowns of both first permanent molars are defective (child about 6 years of age, FPAM 2694 from before 1858).

cusp position of the upper and lower first molars); (2) Hutchinson’s incisors (a short, ill-formed incisal edge of the upper incisors and, less frequently, notching affecting the incisal edge of the lower incisors); (3) Fournier’s or Mulberry molars (expressed by a first molar that is smaller than the second molar and an irregular, poorly formed and pitted occlusal surface of the crown (Fig. 21.7); and (4) canines with a hypoplastic defect circling the tip of the crown (for a complete description see NissankaJayasuriya et al., 2016). Some paleopathological studies have observed variations to these common dental changes associated with congenital syphilis (Ioannou et al., 2015, 2018; Nystrom, 2011). Some of these variations were attributed to the widespread treatment of the disease with mercury, which also causes hypoplastic defects, albeit ones that are substantially different from those caused by congenital syphilis (Ioannou et al., 2015, 2018).

FIGURE 21.5 Dental hypoplasia associated with a case of possible tuberculosis. Hypoplastic lines or spots and possible circular caries are visible in the crowns of all the deciduous teeth (child between 3 and 6 years of age, ANM 2028 from before 1895).

disease was the cause of the disturbance in growth. There is, however, a growing body of bioarcheological literature around the dental changes specific to congenital syphilis. Historic (Nystrom, 2011) and prehistoric (Mayes et al., 2009) evidence for the specific dental changes discussed earlier has been observed in American skeletal assemblages. The positive identification of congenital syphilis from dental changes in pre-15th-century populations in Europe has been used to argue for the presence of the disease in the Old World before contact with the Americas (Gaul et al., 2015; Ioannou et al., 2018), adding to the debate over the origins of this disease (Harper et al., 2011; Meyer et al., 2002). Pathognomonic dental changes have also been used to diagnose congenital syphilis in post-15thcentury European skeletal populations (Lauc et al., 2015).

Abnormal Quantity of Teeth and Dental Crowding

Paleopathology

Pathology

As discussed, EH is a nonspecific indicator of stress and therefore it is not possible to determine if a specific

Developmental defects may result in an abnormal quantity of teeth in the permanent and, less commonly, primary

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FIGURE 21.6 Dental hypoplasia associated with a probable case of tuberculosis. Note multiple hypoplastic lines in the teeth (17-year-old male, FPAM 2016, autopsy 16648 from 1842).

dentitions. Supernumerary teeth (hyperdontia) are defined as teeth that are in excess of the typical 20 deciduous or 32 permanent teeth, but may be accompanied by a deficit in other teeth (Rajab and Hamdan, 2002). This deficit is because the teeth adjacent to the supernumerary teeth may fail to erupt, be malformed (e.g., dilaceration), displaced or affected by root resorption. Ectopic eruption and displacement of supernumerary and original teeth, especially the maxillary canines, is not uncommon in the alveolar region (normotopic) and may occur outside the alveolar region (heterotopic) (Nelson, 2016; Rajab and Hamdan, 2002; Scheiner and Sampson, 1997). Between 0.1% and 3% of populations with European ancestry are affected by supernumerary teeth (Rajab and Hamdan, 2002) and the prevalence is higher ( . 3%) in populations with Asian ancestry (So, 1990). Males are affected approximately twice as frequently as females, but this ratio varies depending on the study population (Scheiner and Sampson, 1997). In the permanent dentition, single supernumerary teeth are most commonly observed (76% 86% of cases), double supernumerary teeth (12% 23% of cases) occur less frequently, multiple supernumerary teeth are rare (,1% of cases), and the

FIGURE 21.7 Dental hypoplasia associated with probable syphilis. (A) Anterior view; note defect of incisal edges of incisors. (B) Occlusal view of mandibular molars. The first molar is smaller than the second and has an abnormal pitted occlusal surface, typical of congenital syphilis (female about 30 years of age, NMNH 219398, dissecting room specimen from before 1903).

condition may occur unilaterally or bilaterally (So, 1990). The anterior maxilla, followed by the mandibular premolar region, are commonly affected by single and double supernumerary teeth, but they may occur elsewhere in the dental arch (Scheiner and Sampson, 1997). The classification of supernumerary teeth is based on form (conical types, tuberculate types, odontome, and supplementary teeth of similar form to a normal tooth) and position in the dental arcade (including mesiodens, paramolars, distomolars, and parapremolars) (Rajab and Hamdan, 2002). The etiology of supernumerary teeth is not clearly understood, but it is thought there is a genetic component to their development (Rajab and Hamdan, 2002). Multiple supernumerary teeth have been associated with certain conditions including Gardiner’s syndrome, cleidocranial dysostosis, growth hormone insensitivity syndrome, and cleft lip and palate (Borges et al., 2013; Scheiner and Sampson, 1997).

758 Ortner’s Identification of Pathological Conditions in Human Skeletal Remains

Teeth may fail to develop, leading to fewer teeth in the dental arcade (tooth agenesis or hypodontia), which is the most common developmental dental anomaly, occurring in between 3% and 11% of individuals depending on population (reviewed by Larmour et al., 2005). The permanent teeth most likely affected by agenesis are third molars, maxillary lateral incisors, mandibular second premolars, mandibular incisors, and maxillary first premolars. Agenesis has also been observed in the deciduous dentition, especially the maxillary and mandibular lateral incisors and may lead to the absence of the subjacent tooth (Larmour et al., 2005). Hypodontia is a multifactorial condition that involves both genetic and environmental factors and is associated with systemic syndromes and other dental anomalies such as microdontia, the impaction of permanent canines, and the transposition of the maxillary first canine and premolar (Larmour et al., 2005; Matalova et al., 2008; Nieminen, 2009). Very rarely, an individual will be affected by both hyperdontia and hypodontia (Anthonappa et al., 2008). Without radiological examination, it is difficult to determine hypodontia from the failure of a tooth to erupt. Tooth eruption is a complex and highly regulated biological process that is not fully understood (Anthonappa et al., 2008; Liversidge, 2006; Wise et al., 2002). Normal eruption times may vary as a result of genetic, sexrelated, and individual factors, and delayed eruption has clinical and paleopathological implications, especially with regard to the correct biological age estimates of children (Halcrow and Tayles, 2008; Suri et al., 2004). A number of factors may cause a tooth to fail to erupt, including the retention of the deciduous teeth (ankylosed primary tooth), a supernumerary tooth, or crowding. An obstruction in the path of an erupting tooth or, less frequently, by the abnormal orientation of the tooth germ, can cause impaction. Impaction is common in mandibular third molars and maxillary canines, but can occur in other teeth (Nelson, 2016; Regezi et al., 2016). Primary failure of eruption is a problem with the propulsive mechanism that moves a tooth (Proffit and Frazier-Bowers, 2009). A number of genetic disorders, including osteogenesis imperfecta, can delay eruption or cause failure to erupt and some individuals may have a genetic predisposition to the condition (Borges et al., 2013; Proffit and FrazierBowers, 2009; Wise et al., 2002). Dental crowding is one of the most common dental anomalies found in modern populations. It is regularly observed in permanent and mixed dentitions, but may also occur within the deciduous dentition (Tsai, 2003). Reasons for dental crowding include the presence of supernumerary teeth, the retention of deciduous teeth, and small arch size compared to tooth size. Certain conditions, such as pituitary dwarfism and growth hormone

insensitivity syndrome, may result in severe dental crowding because bone development, but not tooth formation, is severely disturbed due to the lack of growth hormone (Borges et al., 2013). A number of theories have developed to explain the prevalence of dental crowding in modern populations, including evolution, genetics, and environmental factors (see Mockers et al., 2004; Normando et al., 2012). Although there is an increase in food accumulation and plaque retention with dental crowding, there is little evidence for crowding to become a risk factor for caries development (Hafez et al., 2012).

Paleopathology Evidence for supernumerary teeth, hypodontia, and dental crowding is not uncommon in the paleopathological literature. For example, a study of a Neolithic skeletal assemblage from Poland found evidence for all three conditions, including a supernumerary tooth present in the nasal cavity of one individual (Garłowska, 2001). Supernumerary teeth have also been observed in the nasal cavity and palate (from X-ray identification) of ancient Egyptian individuals from the Dynastic and Pre-Dynastic periods (Satinoff, 1972). Fig. 21.8 is a photograph and X-ray of a heterotopic

FIGURE 21.8 Heterotopic supernumerary canine projecting through left palate. (A) View of palate. (B) Radiograph of hard palate and heterotopic canine (adult skull from Pachacamac, Peru, NMNH 267104).

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supernumerary tooth in the left palate of a prehistoric individual from Pachacamac, Peru. Fig. 21.9 illustrates a historic individual from the Virgin Islands who displays a unilateral, normotopic, supernumerary “fourth molar.” An example of bilateral tuberculate supernumerary teeth between the second and third maxillary molars of an older

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adolescent individual from the 2700-year-old site of Pain Haka, Indonesia, is presented in Fig. 21.10. Tooth agenesis or hypodontia is commonly observed in the paleopathological literature, especially of the third molar. Radiological examination is commonly used to positively identify agenesis from a tooth that failed to erupt. An example of agenesis of the lower lateral incisors of a female individual from South Dakota can be seen in Fig. 21.11. Dental crowding can occur for a number of reasons (discussed earlier). It has been reported that crowding causing malocclusions was rare in prehistory, but severe crowding has been observed in past populations (Mockers et al., 2004). Fig. 21.12 is an example of dental crowding in the maxilla of a prehistoric child from Florida. The alveolar process of this individual is too small for the erupting teeth, leading to the displacement of the incisors.

Abnormal Size of Teeth Pathology FIGURE 21.9 Supernumerary molar on the left side of the mandible (adult female skeleton from an archeological site in the Virgin Islands, NMNH 385695).

Teeth may appear larger than normal in the dentition (macrodontia). Generalized macrodontia may result from a maxilla and mandible that are relatively small compared

FIGURE 21.10 An example of bilateral tuberculate supernumerary teeth between the second and third maxillary molar of an older adolescent individual (burial 45) from the 2700-year-old site of Pain Haka, Indonesia.

760 Ortner’s Identification of Pathological Conditions in Human Skeletal Remains

FIGURE 21.13 Abnormally small maxillary lateral incisors in an adult from Chicama, Peru (NMNH 264518).

FIGURE 21.11 Dental agenesis of the mandibular lateral incisors, occlusal view (adult female from Mobridge site, South Dakota, United States, NMNH 325417).

smaller teeth (e.g., pituitary dwarfism) or from a disproportionally large maxilla and mandible relative to normal-sized teeth (Regezi et al., 2016). Localized or focal microdontia is a relatively common condition that is expressed by a smaller than normal single tooth, often with an altered shape. In descending order, the most common microdonts observed are: (1) peg-shaped maxillary lateral incisors, (2) microdont of the maxillary third molar, and (3) supernumerary teeth (discussed above) (Regezi et al., 2016). Microdontia is closely associated with hypodontia and, similar to hypodontia, is observed in higher frequencies in females compared to males (Larmour et al., 2005).

Paleopathology To researchers familiar with dental assessments of skeletal assemblages, variations in the size of teeth should be easily recognizable. Fig. 21.13 is an example of an adult individual from Chicama, Peru, who displays upper lateral incisors that are smaller than normal. FIGURE 21.12 Severe crowding of the maxillary dentition in a child’s skull, about 10 years of age. Note the displacement of the anterior teeth (specimen is from an archeological site in Canaveral, Florida, United States, NMNH 377496).

to the dentition, or absolute, from a condition such as pituitary gigantism (Regezi et al., 2016). An abnormally large tooth or a group of teeth is known as focal or localized macrodontia. For example, third molars may be affected by macrodontia, although this is relatively uncommon (Regezi et al., 2016). Microdontia is a condition where the teeth appear smaller than normal. The generalized form of the condition affects the entire dentition due to the formation of

Dental Anomalies Pathology There is considerable, normal variation in the shape of the teeth that is genetically controlled. These morphological variations of the crown and root, also known as nonmetric traits, commonly include shovel-shaped incisors, Carabelli’s cusp, supernumerary roots, and molar cusp number and are used to assess ancestry (for an in-depth review, see Scott, 2008). Developmental dental anomalies are observed in modern populations relatively frequently. Fusion and gemination of teeth are developmental conditions that lead to similar expressions in fully formed teeth in both the primary and

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permanent dentitions (Ravn, 1971; Regezi et al., 2016). Gemination occurs as a result of the development of two teeth from one tooth germ. This can cause partial cleavage, where the two crowns share a root canal, or complete cleavage (twinning), where two teeth arise from the same tooth bud (Grover and Lorton, 1985). In contrast, the joining of two developing tooth germs is known as fusion (More and Tailor, 2013). This may result in purely root fusion of the dentin and cementum, leaving two separate crowns, or the fusion of the whole root/crown length (Regezi et al., 2000). In fusion, the root canals may be separate or shared, which may lead to difficulties in differentiating between fusion, gemination, and supernumerary teeth, although radiological examination can help with interpretations (Altug-Atac and Erdem, 2007; Regezi et al., 2000). The etiology of fusion and gemination is unknown, but trauma has been suggested as a potential cause for both conditions (Regezi et al., 2016). Concrescence is a condition defined by the joining of two tooth roots by hyperplastic cementum, which may occur during, or after, eruption. Rarely, a tooth root may attach to an impacted tooth crown by the same mechanism (Sugiyama et al., 2007). Concrescence is commonly observed between the maxillary second and third molars and is thought to be a result of trauma and overcrowding (Regezi et al., 2016). Other commonly observed dental anomalies include enamel pearls, dilaceration, and, less frequently, taurodontism. Enamel pearls are a developmental defect expressed as a small round deposit of ectopic enamel on the bifurcation or trifurcation of molars or premolars, but may also be located on single-rooted premolars (Chrcanovic et al., 2010; Regezi et al., 2016). They are most commonly observed in the maxillary, followed by the mandibular, molars (Chrcanovic et al., 2010; Risnes, 1974). Enamel pearls may form on the surface of the tooth (extradental) or in the dentin proper (intradental) (Ortner, 2003). Dilaceration is an extreme angulation of the tooth root that is believed to arise from trauma during tooth development (Regezi et al., 2016). Taurodontism is recognized by the enlargement of the pupal chamber in the apical/occlusal aspect. It is caused by an enlargement of the crown or displacement of the pulpal floor and lack of constriction at the cemento enamel junction. Taurodontism is most prevalent in permanent molars, but has been observed in both primary and permanent dentitions and in any tooth and quadrant (Jafarzadeh et al., 2008). Prevalence rates vary between populations and it has been found in higher frequencies in Middle Eastern and First Nations groups. Taurodontism is associated with a number of genetic

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FIGURE 21.14 Fusion of mandibular right incisors (Native American child about 1 1/2 years of age from a historic period site in Nebraska, United States, NMNH 243355).

FIGURE 21.15 Fusion of the mandibular deciduous right lateral incisor and canine (child, about 8 years of age, from an archeological site in New Mexico, United States, NMNH 269221).

conditions, including Down syndrome, and has also been observed in Neanderthal dentitions (Jafarzadeh et al., 2008; Regezi et al., 2000).

Paleopathology Fig. 21.14 illustrates fusion between the central and lateral right incisors in a 1.5-year-old child from the historic period in Nebraska, United States (NMNH 243355). The second case is from an archeological site in New Mexico, United States (NMNH 269221), and involves the deciduous mandibular right lateral incisor and canine (Fig. 21.15) of an 8-year-old child. A radiograph indicates that the roots were fused, as well. The third case is from the permanent dentition of an adult individual from an archeological site in New Jersey, United States (NMNH 285307). Fusion has taken place between the right lateral incisor and canine, and created a very large tooth, which might, on superficial inspection, be confused with an abnormally large tooth rather than fusion of two teeth. The roots of the two teeth are also fused (Fig. 21.16).

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FIGURE 21.16 Fusion of the permanent mandibular, right lateral incisor, and canine (arrow). An X-ray film reveals that the roots are fused. This fusion should be distinguished from abnormally large teeth (macrodontia) (specimen is from an archeological site in New Jersey, United States, NMNH 285307).

An enamel pearl can be observed on the distal surface of the roots of the left second and third molars in Fig. 21.17. The growth encroached on the alveolar bone, creating a noticeable marked cavity adjacent to the second molar but only a slight depression adjacent to the third molar.

Dental Discoloration Pathology There are three main types of dental stains or discolorations: extrinsic, intrinsic, and internal (Watts and Addy, 2001). Extrinsic staining is usually a result of environmental factors such as diet and drug use. For example, coffee, tea, tobacco and betel nut (Areca catechu) commonly cause staining to tooth surfaces (Watts and Addy, 2001). It is also thought that chromogenic bacteria may stain teeth brown, black, green, and orange, and this is primarily observed in children (Regezi et al., 2016). Intrinsic stains are a result of an issue, such as hereditary conditions or metabolic disease (including rickets) and ‘systemically circulating substances’ during amelogenesis that affects the thickness or composition of the enamel (Regezi et al., 2016; Watts and Addy, 2001). In modern times, tetracycline is a major cause of intrinsic staining of both the deciduous and permanent teeth because of its ability to bind with calcium. A high fluoride intake during deciduous or permanent tooth development may result in fluorosis, frequently observed as flecking or diffuse opacious mottling that ranges from white to black/brown in color (Watts and Addy, 2001). A number of other conditions may cause intrinsic staining,

FIGURE 21.17 Enamel pearls on the distal root surface of the mandibular, left permanent second and third molars. (A) Molars, in situ; note that the enamel pearls encroach on the alveolar bone. (B) Detail of enamel pearl on the second molar (specimen from an archeological site in South Dakota, United States, NMNH 325367).

especially of the deciduous teeth, including Rh incompatibility (erythroblastosis fetalis), congenital porphyria, liver disease, biliary atresia, and neonatal hepatitis (Regezi et al., 2016). As discussed previously, amelogenesis imperfecta may manifest as an abnormally thin (hypoplastic) layer of enamel or a hypomineralized (lack of, or poor, mineralization) area of enamel, where thickness is unaffected but extreme softness increases (Hu et al., 2007). Hypomineralized enamel may be expressed as an intrinsic stain on the tooth by a chalky spot or opacity. In both hypoplasia and hypomineralization, the affected area may be more susceptible to decay, as in the case of circular

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TABLE 21.1 Abnormal Conditions Resulting in Discoloration of the Teeth, With Typical Pattern and Color Change (Based Primarily on Pindborg, 1970: 211 224) Cause of discoloration

Pattern

Color

Fluorosis

Mottled

Yellow to brown

Congenital heart disease

Diffuse

Bluish white

Erythroblastosis fetalis

Diffuse

Green to yellow, brown or gray

Neonatal hepatitis

Diffuse

Yellowish brown

Congenital defect of bile duct

Diffuse

Green (particularly the roots)

Porphyria

Striated

Pinkish brown (roots indigo)

Hemorrhage or necrosis of pulp

Diffuse

Light brown to gray

Tobacco

Diffuse

Brown

Betel

Diffuse

Dark brown (occlusal surface and roots tend not to be affected)

caries. Enamel can undergo hypomaturation, which manifests by way of discolored (brown to yellow) crowns with dentin-like tissue density (Hu et al., 2007). Dentinogenesis imperfecta (DI) also results in extreme tooth staining, beginning with blue- or brown-colored teeth that rapidly degrade and wear (Watts and Addy, 2001). Internalized discoloration is a process of external staining that affects a tooth after development in the areas of an enamel defect or exposed dentin. The stain may be incorporated in a developmental defect, such as a hypoplasia, in patches of dentin exposed by tooth wear, on tooth roots exposed by gingival recession, in or around caries, or on restorative dental material (Watts and Addy, 2001).

Paleopathology Table 21.1 lists possible conditions and their associated expression of staining (pattern and color) that may be found in archeological samples, including fluorosis, congenital heart disease, erythroblastosis fetalis, neonatal hepatitis, congenital defects of the bile duct, porphyria, hemorrhage or necrosis of the pulp, and the use of tobacco and betel nut. Because many types of staining may appear similar, careful attention needs to be paid to the color and distribution of the stain to identify whether it is extrinsic, intrinsic, internal, or, possibly, taphonomic in nature. Extrinsic staining remains on the teeth in many burial environments. A number of researchers have identified likely betel staining, caused by the leaf of Piper betle, on the teeth of prehistoric individuals from Southeast Asia and the Pacific (Douglas et al., 1997; Oxenham et al., 2002b; Pietrusewsky et al., 1997). Recently, new methods using ultra-high-performance liquid chromatography mass spectrometry have been used to positively identify nicotine in dental calculus, even when staining

was not always observed (Eerkens et al., 2018). Differentiating hypomineralization from chemical staining as a result of taphonomic effects in the burial environment can be difficult. Methods using Raman spectroscopy, Xray microcomputed tomography, X-ray fluorescence (Garot et al., 2017), inductively coupled plasma-atomic emission spectroscopy, and scanning electron microscopy-energy dispersive X-ray analysis (SEM-EDX) (Brown et al., 2014), have successfully differentiated between postmortem and antemortem staining.

IDENTIFYING DENTAL WEAR AND ORAL DISEASE Oral pathology provides an opportunity to evaluate oral health between different individuals and within and among different populations. It is imperative that interpretations are grounded in an understanding of the demography of the assemblages, and are most informative when contextualized with a multifactorial consideration of other oral pathologies due to the recognized synergistic relationship in the oral biome (Broadbent et al., 2011; Hillson, 2001; Larsen and Fiehn, 2017). Evaluating oral health in this context allows for a deeper understanding of potential sex-based differences in the prevalence and the age-progressive nature of oral disease. There are a multitude of comprehensive syntheses of oral health in bioarcheology (Hillson, 2013; Irish and Scott, 2016; Larsen, 2015; Pinhasi and Mays, 2008). As Wood et al. (1992) predicted and DeWitte and Stojanowski (2015: 418) reiterated, advances in the fields of human biology, demography, epidemiology, and genetics have significantly contributed to our knowledge, and bioarcheological interpretations should be

764 Ortner’s Identification of Pathological Conditions in Human Skeletal Remains

grounded in clinical evidence pertaining to oral health. The following sections describe dental wear and oral pathologies from clinical followed by bioarcheological perspectives.

Dental Wear Pathology Although there is variability in the definition of dental wear in the clinical and paleopathological literature, here we follow Burnett’s (2016: 215) definition of “wear” as “the resulting loss of tooth hard tissue from any combination of attrition, abrasion and corrosion.” Mechanical stresses exerted from tooth-on-tooth contact during the mastication of food and tooth grinding (bruxism) will result in the wear of the occlusal and interproximal surfaces of the tooth crown, known as attrition (Hillson, 2008). Attrition is recognizable by distinctive matching wear facets from the continuous contact of opposing teeth (maxilla vs mandible) or adjacent teeth in the same arch. Certain wear patterns are characteristic of attrition, such as more pronounced wear on the lingual aspect of the maxillary teeth and buccal/labial surfaces of the mandibular teeth (Burnett, 2016). Approximal, or interstitial, attrition occurs in the interproximal space of two adjacent teeth from the slight movement of teeth that accompanies chewing. This wear creates the interproximal contact facets used to help identify specific teeth, but rarely if ever exposes the dentin (Ortner, 2003). The well-defined wear facets on the crown of the teeth differentiate attrition from abrasion, which is characterized by more dispersed wear across a diffuse surface or localized area of dental tissue (Burnett, 2016). Abrasion develops when the teeth come into contact with food or other foreign objects, including inclusions in food (e.g., sand and grit). Extramasticatory behavior, such as processing plants or hides for material, food preparation, pipe smoking, and some types of oral hygiene can also cause very specific patterns of abrasion (Irish and Turner, 1997; Larsen et al., 1998; Lukacs and Pastor, 1988; Milner and Larsen, 1991; Molnar, 1972; Pindborg, 1970). Dental corrosion, or erosion, is the chemical dissolution of both enamel and dentin in the absence of bacteria (d’Incau et al., 2012; Keiser et al., 2001). It can cause wear patterns similar to attrition and abrasion, such as dentin scooping. However, any surface of the tooth may be affected by corrosion, and the lingual surfaces of the anterior teeth are particularly vulnerable. Dental corrosion can result from the consumption of acidic foods or, as commonly seen in clinical settings, regurgitated stomach acids resulting from acid reflux, eating disorders, or alcoholism (Holbrook et al., 2009; Lussi and Jaeggi, 2006; Regezi et al., 2016). Although attrition and abrasion are the most common types of wear, they do

not usually occur independently of each other or corrosion (when present), and biological and behavioral variation will dictate the expression of each type of wear (Kaidonis, 2008). As tooth wear progresses, teeth will move to maintain occlusion, leading to continued eruption, mesial drift and shortening of the dental arch, lingual tipping, and remodeling of the temporomandibular joint (d’Incau et al., 2012; Kaidonis, 2008). Extreme tooth wear that results in these changes (and others, such as a reduction in overbite and overjet) may lead to an edge-to-edge bite (labiodontia) from a “normal” scissor-bite (psalidontia) (d’Incau et al., 2012). Other factors, such as ante-mortem tooth loss (AMTL) causing tooth migration and malocclusion, weak structural integrity of the apatite crystals in the enamel, and the chemical composition of food may also influence the rate and pattern of tooth wear (Molnar and Molnar, 1990; Oxenham et al., 2002a). The abnormal position of teeth can cause localized wear on the affected teeth, known as pathologic attrition. Tooth wear is a natural process that increases with advancing age and is not pathological unless the wear becomes severe enough that the pulp cavity of the tooth is exposed. When this occurs, odontoblasts in the dentin respond by forming secondary dentin to protect the pulp cavity. If tooth wear occurs faster than the rate at which secondary dentin is deposited, the pulp and associated alveolar bone will be exposed to possible infection (Ortner, 2003). Tooth wear has the potential to destroy certain morphological attributes of a tooth and introduce bias into ancestry studies that use nonmetric dental traits (see review by Burnett, 2016).

Paleopathology The severity of tooth wear, especially attrition and abrasion, is influenced by advancing age. Methods have been developed to estimate the age of adults from the patterns of tooth wear between certain teeth, especially the molars (e.g., Benfer and Edwards, 1991; Brothwell, 1981; Mays, 2002; Walker et al., 1991). Early studies of tooth wear first identified a correlation between food type and the extent of tooth wear of prehistoric individuals, linking the pattern and severity of the wear to certain diets and food preparation techniques (Molnar, 1971, 1972; Smith, 1984). Standard methods are used to identify the extent of tooth wear in a skeletal sample. Commonly used methods include those of Scott (1979), which grades the extent of wear in each molar quadrant, and Smith (1984) and Molnar (1971) who detail the destruction of crown enamel and the extent of dentin exposure for the entire dentition. The identification of severely worn teeth can potentially provide information about the etiology of other oral pathologies. A number of studies classify “severe” tooth wear as a pathological

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FIGURE 21.18 Severe attrition of the mandibular incisors and canines with exposure of secondary dentin. The pulp cavities of the left lateral incisor and left canine are exposed; both teeth have an alveolar lesion (adult male from archeological site at Puye, New Mexico, United States, NMNH 262957).

condition in itself because the exposure of the pulp cavity from wear leaves the tooth vulnerable to infection and potential exfoliation (Domett, 2001; Lukacs, 1989; Tayles, 1999). Fig. 21.18 is an example of severe attrition complicated by pulp cavity exposure and alveolar lesions in the dentition of an adult male from the pre-Columbian site at Puye, New Mexico, United States (NMNH 262957). The maxilla, the incisors, and canines are present but badly worn. The incisors have exposed secondary dentin and the canines have wear exposing the pulp cavity on the left. On the mandible, the central incisors are missing antemortem, as apparently are the third molars. The remaining incisor crowns are worn away with exposure of secondary dentin. The canine crowns are almost worn away. There is pulp exposure of the left lateral incisor and left canine, with an alveolar lesion associated with both teeth. The crown of the left first premolar has been destroyed by caries.

Caries Pathology Caries is a complex multibacterial, multifactorial disease, which is caused by a synergistic relationship between many factors (Mira et al., 2017). Although historically Streptococcus mutans and Streptococcus sobrinus have

765

commonly been linked to the etiology of caries (Loesche et al., 1975; Loesche, 1986), recent advances in molecular approaches have demonstrated the composition of the polymicrobial biofilm is much more complex (Chapple et al., 2017; Gross et al., 2012; Krzy´sciak et al., 2016; Simo´n-Soro et al., 2014; Simo´nSoro and Mira, 2015; Zaura and Ten Cate, 2015). The etiology of caries currently is understood best from the perspective of the ecological plaque hypothesis (Kilian et al., 2016; Marsh et al., 2015; Marsh, 2003; Sim et al., 2016), where caries susceptibility is a complex interplay and balance between plaque ecology and the host (Sim et al., 2016). The consumption of carbohydrates reduces the pH of the plaque biofilm that creates an acidogenic enabling environment of acid-producing and acid-tolerant bacterial colonies, which leads to an increased production of demineralizing acid (Marsh et al., 2015; Zaura and Ten Cate, 2015). Many of the dynamic processes occurring in the oral biome involved in the initiation of carious lesions occur at a microscopic level, and may be mitigated by the actions of attrition, abrasion, and erosion (Heymann et al., 2013; Holmen et al., 1987; Kumar, 2011); lesions of the enamel are the final sequela. Incipient caries begins as demineralization below the surface of the tooth, only visible at a microscopic level (Botta et al., 2016; Jones and Boyde, 1987; Lautensack et al., 2013). The macroscopic manifestation of lesions begins as a small opacity, progressing through several phases, increasing in size and intensity, and eventually causing necrosis of the dentin and pulp chamber. The pathogenesis of caries is slow and dynamic, cycling through static and active phases (Fejerskov et al., 2015; Heymann et al., 2013; Pine and ten Bosch, 1996). There are three types of caries: active, acute, and chronic (Fejerskov et al., 2015; Heymann et al., 2013). Carious lesions generally follow patterns in their predilection of tooth type due to the accumulation of biofilm as a function of occlusal morphology, where the efficacies of attrition, abrasion, or erosion are reduced (Fejerskov et al., 2015; Klein and Palmer, 1941; Macek et al., 2003; Sheiham and Sabbah, 2010). In terms of sex differences, much of the clinical literature suggests a female predisposition to higher caries prevalence (Haugejorden, 1996; Jain and Kaur, 2015; Kamate et al., 2017; Silva de Araujo Figueiredo et al., 2017). Root caries can occur as a result of periodontal disease, which effectively reduces the surrounding alveolar margin, facilitating exposure of the roots (Heymann et al., 2013). Passive eruption or overeruption can also predispose the dentition to root caries (d’Incau et al., 2012; Newman, 1999; White and Pharoah, 2014). Root caries is one of the primary causes of AMTL in older adults (Heymann et al., 2013).

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Paleopathology Although caries is one of the most commonly recorded pathologies in bioarcheological assemblages, the techniques used for identification, recording, and analysis have lacked consistency (Hillson, 2001). Hillson (2001) recommends recording the position and prevalence of lesions in addition to recording caries by sex and age, as the maxillary and mandibular dentition have a differential susceptibility to caries (Thylstrup and Fejerskov, 1994). Two examples demonstrate the differential positions of carious lesions. Fig. 21.19 shows interproximal caries manifesting on all of the interproximal surfaces of the maxillary incisors of an adult male from the Shannon site in Virginia, United States (NMNH 382419). Fig. 21.20 illustrates classic root caries on the mesial interproximal surface of the lower left first molar of an adult female from Puye, New Mexico, United States (NMNH262944). There is moderate alveolar resorption indicated by the distance between the cemento enamel junction and the alveolar bone, suggesting soft-tissue recession, which would have exposed the tooth root to bacteria, predisposing the individual to caries. It is also important to take into consideration patterns of tooth wear, chipping and fractures, and cultural modifications of teeth when recording carious lesions since most carious lesions are recorded when a macroscopically observable cavitation is present. It is common for lesions to be recorded as present or absent per tooth, however, caries may manifest in several different locations on one tooth, each of these with a potentially different underlying etiology, so it is important to record multiple incidences (Hillson, 2001). The complex synergistic relationship among oral pathologies is widely acknowledged (Broadbent et al., 2011; Hillson, 2001; Larsen and Fiehn, 2017). Severe tooth wear, caries, pulp exposure and alveolar lesions influence the underlying etiology of AMTL and potentially the loss of information on carious lesions. Because of the complexity within the oral environment, several methods have been developed to try to retrospectively predict the effects of multiple etiological variables (Duyar and Erdal, 2003; Erdal and Duyar, 1999; Lukacs, 1995). These methods have largely fallen out of favor in bioarcheology since the observed caries rates may not be an accurate representation of the life history of caries in an individual. These data, however, are based on observations, as opposed to transformed data, and are more easily comparable among and between assemblages. If a comprehensive recording scheme is followed, such as proposed by Hillson (2001), the interaction between these oral pathologies should be highlighted, elucidating probable causal interactions within the oral environment.

FIGURE 21.19 Interproximal caries of the maxillary incisors (adult male from a Late Woodland site in Virginia, United States, NMNH 382419).

FIGURE 21.20 Root caries of the mesial, interproximal surface of the lower left first molar. Note the evidence of moderate alveolar resorption indicated by the distance between the cemento enamel junction and the alveolar bone. The soft tissue would have receded with the bone, exposing the tooth root to the bacteria causing caries (anterolateral view of mandible) (adult female from the archeological site of Puye, New Mexico, United States, NMNH 262944).

Historically, caries has been used to evaluate one aspect of oral health among and between populations engaging in different subsistence practices during various temporal periods, in different geographic locations, and during transitions in human prehistory (Cohen and Crane-Kramer, 2007; Larsen, 2015). There are variations in patterns geographically and chronologically, both within and between subsistence economies. However, the general trends in these data indicate that huntergatherers had fewer caries than later agricultural populations, which has been broadly interpreted as poorer oral health after the transition to agricultural subsistence (Larsen, 2015). The interpretations of sex differences in caries prevalence have been interpreted using behavioral dietary

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models. However, there has been a shift to considering clinical-based literature in these interpretations and focusing on multifactorial analyses to provide more nuanced understandings. The recent increase in the use of stable isotopes in bioarcheology provides an opportunity to evaluate whether there were actual differences in diet between the sexes or within or among different populations (Bonsall and Pickard, 2015; Petersone-Gordina et al., 2018; Tomczyk et al., 2013).

Alveolar Lesions Pathology The pathogenesis of alveolar lesions is contingent on the underlying etiology and will manifest in different ways. Exposure of the dental pulp can cause inflammation within the alveolar bone in the form of a periapical granuloma. These periapical granulomas are the result of accumulated granulation and the resorption of bone, presenting as a lesion with smooth edges (Rajendran and Sivapathasundharam, 2012). Periapical cysts, also known as radicular cysts, are usually the sequela to periapical granulomas, and are the result of a bacterial infection due to necrosis of the pulp. They manifest as epithelium-lined lesions associated with accumulated fluid and resorption of bone, presenting as a larger lesion than a periapical granuloma (Rajendran and Sivapathasundharam, 2012). Both granulomas and cysts are relatively symptomless and cause little discomfort in life (Rajendran and Sivapathasundharam, 2012). The resulting lesions from periapical inflammation will have different characteristics based on the duration of the infection and whether it is pyogenic. An acute infection produces a pressurized swelling that ruptures and is usually painful and accompanied by fever. A chronic infection produces a periapical abscess with rough edges and a sinus or channel, but does not cause pain (Rajendran and Sivapathasundharam, 2012). The distinction between these lesions is not straightforward for either clinicians nor bioarcheologists; it requires microscopic examination (Eversole, 2011; Rajendran and Sivapathasundharam, 2012). In contemporary populations alveolar lesions associated with infection of the tooth pulp and the inflammation of periapical tissue has been one of the major causes of tooth extraction (Hillson, 2005). Clinical evidence suggests that females are more predisposed to oral lesions (Armitage, 2013; Jain and Kaur, 2015).

Paleopathology There has been a lack of standardized nomenclature used to define and evaluate alveolar lesions in bioarcheology

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(Dias et al., 2007; Ogden, 2008). The term alveolar lesions is used to broadly encapsulate lesions of the alveolar bone with no intimation as to the underlying etiology or pathogenesis. Alveolar lesions are the varying manifestations of an infection of the dental pulp, which may have been caused by caries, attrition, or trauma. Fig. 21.21 is an example of an adult male individual from Puye, New Mexico (NMNH262948), who exhibits alveolar lesions associated with gross dental caries exposing the dental pulp of both first molars. Fig. 21.21A illustrates the occlusal view of the maxilla. The left central incisor is missing postmortem, the alveolar bone of the right second premolar and third molar demonstrate alveolar resorption and remodeling indicative of AMTL. Fig. 21.21B illustrates the anterior view of the maxilla demonstrating alveolar lesions associated with the first molars and the right premolar. Also, see Fig. 21.18 (referenced earlier) as an example of alveolar lesions as a consequence of pulp exposure due to severe attrition.

FIGURE 21.21 Dental caries with destructive lesions penetrating the pulp cavity of both first molars. (A) Occlusal view; left central incisor missing postmortem. Right second premolar and third molar sockets show evidence of alveolar remodeling suggestive of antemortem tooth loss. There is an alveolar lesion associated with the premolar. (B) Anterior view of maxilla, showing alveolar lesions associated with the first molars and right second premolar (adult male from archeological site near Puye, New Mexico, United States, NMNH 262948).

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The infection of dental pulp is transmitted down the root, through the apical foramen and into the periapical alveolar bone. The resulting lesion is a consequence of the temporal nature of the inflammatory response. Alveolar lesions are commonly misdiagnosed as abscesses in bioarcheology, however, it is more likely that they are periapical granulomas or cysts. There are bioarcheological guidelines for the identification and differentiation of alveolar lesions (Dias and Tayles, 1997; Dias et al., 2007; Ogden, 2008) which are summarized below; in paleopathology the specific etiology of the lesion is not as important as noting the amount of bone lost, as this has possible implications in the etiology of AMTL. Acute periapical infections that progress through inflammation and reparation, and naturally resolve, would be difficult to identify in skeletal material (Dias and Tayles, 1997). Periapical granulomas are caused by osteoclastic activity as a result of chronic infections and manifest as a well-delineated alveolar lesion with smooth walls. If the source of the infection is removed, a periapical granuloma may resolve; however, if the infection is chronic and progressive, an apical cyst may develop from the granuloma, and once a cyst is present it will not regenerate even if the source of the irritation is removed (Dias and Tayles, 1997; Dias et al., 2007; Ogden, 2008). Apical cysts are also characterized by smooth-walled lesions, however, they are larger in size and progressively expand. Discriminating between periapical granulomas and cysts diagnostically in skeletal remains is not possible. However, as periapical granulomas are small, it has been suggested anything larger than 2 3 mm in diameter at the maximum intrabony margins would likely represent an apical cyst (Dias and Tayles, 1997; Dias et al., 2007). Periapical abscesses are the result of acute infection and are characterized by an accumulation of pyogenic material in a soft-tissue cavity. As a consequence of their acute nature, there is no osteoclastic involvement and therefore no resorption of bone (Dias and Tayles, 1997). The infection within the soft tissue causes swelling until it ruptures and discharges the pyogenic material through either existing vascular canals or perforations in the bone. Once the pyogenic material is discharged and the infection has dissipated, the connective tissue regenerates, leaving no sign of the infection. These are, therefore, difficult to identify in skeletal material (Dias and Tayles, 1997). If the periapical abscess develops within a periapical granuloma or cyst, they may roughen the smoothness of the walls of the preexisting lesion; this would be observable microscopically in skeletal remains (Dias and Tayles, 1997). If the infection persists and becomes chronic in nature, osteoclastic activity will occur in the formation of sinuses or fistulae within the alveolar to discharge the pyogenic material and alleviate the swelling. Chronic abscesses can be differentiated from other alveolar lesions through the observation of

a bony sinus or interconnecting fistulae in skeletal remains (Dias and Tayles, 1997). In summary, in terms of a differential diagnosis of alveolar lesions, a periapical granuloma manifests as a small circumscribed lesion less than 3 mm with smooth walls, an apical cyst is characterized by the same features but is more than 3 mm in diameter. If the walls of the lesion are not smooth, it indicates the secondary development of an acute abscess within the granuloma or cyst. A primary chronic abscess is characterized by a small lesion with roughened walls and sharp margins with associated sinuses or fistulae (Dias and Tayles, 1997; Dias et al., 2007).

Other Miscellaneous Conditions of the Oral Cavity Pathology There are numerous other types of pathologies that may affect the maxilla and mandible and, potentially, other parts of the skeleton. Because of their intimate relationship to the teeth and bony changes in the skull, a few of the more common lesions that are found exclusively in the jaws will be discussed. The expression of a number of these pathologies may appear similar during macroscopic analysis, and radiological analyses may provide a better diagnostic tool in some instances. Regezi et al. (2000: 86 96) provide a helpful summary of jaw abnormalities for the reader interested in more comprehensive coverage of the subject.

Odontogenic Cysts: Pathology and Paleopathology Odontogenic cysts are infections that occur in or around a tooth and include radicular, or periodontal cysts (discussed earlier), dentigerous cysts, and primordial cysts (Koseoglu et al., 2004; Regezi, 2002). After radicular cysts, dentigerous cysts are the most common type of odontogenic cyst and are likely a result of developmental problems causing the proliferation of the enamel organ remnant after crown formation, from the tooth bud of permanent or supernumerary teeth (Asaumi et al., 2004; Koseoglu et al., 2004; Regezi et al., 2016). Dentigerous cysts can cause the displacement of the unerupted tooth and the resorption of the roots of adjacent teeth, and can result from trauma, developmental syndrome, or systemic disease (Freitas et al., 2006). They are more frequently observed in the mandible than the maxilla (Kasat et al., 2012). This type of cyst is common around impacted third molars and may spread along the body of the mandible or into the ramus (Freitas et al., 2006; Ortner, 2003). In the maxilla, a dentigerous cyst affecting the canine or molars may extend into the maxillary sinus or orbital floor and may, infrequently, cause ectopic eruption of the tooth into

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these areas (Buyukkurt et al., 2010; Kasat et al., 2012). In dry bone, this type of cyst would appear as a cavity that is not intimately associated with a dental root, a possible enlargement of the overlying cortex and an association with the crown of the affected tooth if it is still intact postmortem (Ortner, 2003). There is debate over the classification of odontogenic keratocysts and keratocystic odontogenic tumors, and both names have been used to describe a proliferating cyst that develops from the remnants of the dental lamina (Regezi et al., 2016; Thompson, 2014). They occur at any age but are frequently observed in individuals in their 20s and 30s and may reoccur. They may present as solitary or multiple cysts. The mandible is affected more than the maxilla (2:1), frequently in the area of the third molar where the mandibular ramus may be affected. Similar to a dentigerous cyst, odontogenic keratocysts/keratocyst tumors will appear as a cyst not intimately associated with a tooth root, which may be multilocular or unilocular and may or may not be associated with a crown of an adjacent tooth (Regezi et al., 2016).

Odontogenic Tumors: Pathology and Paleopathology There are a number of odontogenic tumors that may arise from the epithelial or mesenchymal components of the dental bud (Ortner, 2003). One type is an ameloblastoma, that originates in the odontogenic epithelium during childhood or adolescence and continues to progress later in life. It is usually a benign tumor that affects the mandible more frequently than the maxilla, commonly in the area of the third molar (Mendenhall et al., 2007). The invasive, proliferating tumor presents as a cystic mass when developed, often multiloculated, which expands the bone but maintains a thin, ridged, bony shell. Enamel is not formed by the tumor tissue, and a tooth is not included in the lesion (Ortner, 2003). The other odontogenic tumors are of mesenchymal origin such as the odontoma, a tumor composed of dental tissues that have proliferated in an irregular way. An odontoma may present as complex, with all three dental tissues (mostly dentin, but also cementum and enamel) present as “toothlets” common in the anterior maxilla—or compound, where there is no differentiation between the dental tissues, and is usually observed in the posterior maxilla or mandible (Amado et al., 2003). Abnormal development of the cementum may result in a so-called “cementoma,” an umbrella term to describe a number of tumors of the cementum that may affect one or multiple adjacent teeth, including benign cementoblastomas and gigantiform cementomas (Matsuzaka et al., 2002). Fibro-osseous lesions of the jaw may also result in bony changes, including the relatively rare, odontogenic fibroma (Regezi, 2002). This appears in

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dry bone as a smooth-walled, more or less enlarged, lytic defect without any identifiable characteristics (Ortner, 2003).

Nonodontogenic Cysts and Tumors: Pathology and Paleopathology Previously, a number of nonodontogenic cysts, including globulomaxillary cysts and median mandibular cysts, were considered fissural cysts—arising from the “entrapment” of the epithelium during the “fusion” of the midline of the mandible or the premaxilla and maxillary processes. These are now considered a part of the spectrum of odontogenic cysts and tumors (Regezi et al., 2016). Benign fibro-osseous lesions (BFOLs) of the craniofacial skeleton are a group of poorly defined conditions that are expressed as hypercellular fibroblastic stroma and may contain bone and other calcified tissue like cementum (El-Mofty, 2014; Eversole et al., 2008). BFOL are associated with fibrous dysplasia, a condition where normal-growing bone is replaced by poorly mineralized and inadequately organized immature bone. It can occur on multiple (polyostotic) or singular bones (monostotic) and, in the case of the latter, may affect the maxilla or mandible (El-Mofty, 2014). Recognition of such lesions in dry bone would depend on good preservation of fragile trabecular bone (Ortner, 2003). A variety of lytic conditions, such as eosinophilic granuloma, “brown tumor” of hyperparathyroidism (Proimos et al., 2009), giant-cell reparative granuloma (Palacios and Valvassori, 2000), or metastatic carcinoma (Hirshberg et al., 2014) can affect the jaws. In dry bone, such lesions are devoid of identifying characteristics in themselves but may be interpretable in the context of findings elsewhere in the skeleton. Carcinoma of the oral or nasal cavity, the paranasal sinuses, and even the facial skin may cause extensive destruction of a jaw or other facial bone by direct invasion. As a rule, the lesion would show a frayed margination in dry bone with little, if any, osteosclerotic reaction (Ortner, 2003).

Hyperostosis/Tori: Pathology and Paleopathology Hyperostosis is characterized by abnormal bony growths present on the longitudinal ridge of the hard palate or lingual surface of the mandible. The torus palatinus is the maxillary form of the condition and is expressed as flat, nodular, spindle-shaped, and lobular. The torus mandibularis occurs on the mandible (commonly in the canine or premolar region), either unilaterally or bilaterally, and its shape is more amorphous and not as easily classified as the torus palatinus (Fig. 21.22) (Loukas et al., 2013). Buccal and palatal exostoses are similar to tori in that they are hyperplastic bony nodules of mature trabecular

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In modern epidemiological studies, molars are lost more frequently than the anterior teeth or premolars as a result of periodontitis (Oliver and Brown, 1993). Clinical evidence demonstrates females are more predisposed to AMTL (Russell et al., 2008; Silk et al., 2008). Not surprisingly, AMTL is usually correlated with increasing age as dental pathologies and risk of trauma also increase with age.

Paleopathology

FIGURE 21.22 Lingual hyperostosis of the mandible (no data).

and cortical bone, but they are located in different areas of the mouth and are less frequently observed than tori. Buccal exostoses are found on the buccal aspect of the mandible or maxilla and commonly near the premolars and molars. Palatal exostoses are found on the maxilla near the palatal tuberosity (Jainkittivong and Langlais, 2000). The etiology of the exostoses and tori is not known, but the higher prevalence of the conditions in some populations suggests that there may be a genetic predisposition and environmental, functional, and agerelated factors have also been suggested. Both tori and exostoses are benign and asymptomatic and there does not appear to be any negative health consequences regarding these conditions (Jainkittivong and Langlais, 2000; Loukas et al., 2013).

Antemortem Tooth Loss Pathology Permanent teeth may be lost prematurely through trauma, chronic pathology, or intentional ablation. As discussed earlier, the final culmination of a range of oral pathologies is tooth loss. This may be a sequela to gross caries, root caries, pulp chamber exposure and periapical infection, severe attrition with continuous eruption, or periodontal disease. In extremely worn teeth, which have continued to erupt, the socket may be shallow and remodeled, with the root held in place only by the gingiva. This would be represented by a shallow, remodeled alveolus and tooth roots. Intentional removal of teeth, not otherwise associated with tooth extraction, is termed tooth ablation. The distinction between intentional removal and pathological tooth loss is not always possible. An examination of the pattern of AMTL in individuals is required to investigate possible ablation as intentional removal will often be symmetrical or patterned (Burnett and Irish, 2017b).

In bioarcheology, AMTL can be differentiated from postmortem tooth loss, the latter characterized by the presence of alveoli with no evidence of remodeling (Burnett and Irish, 2017a). A differential diagnosis of AMTL requires careful consideration of the alveolar bone and the adjacent dentition to differentiate between AMTL due to underlying pathology, accidental trauma, underlying genetic factors such as agenesis or impaction, or intentional culturally-induced ablation. The presence or absence of a residual space between teeth and of wear facets on adjacent teeth can inform on whether there was preexisting dentition that has subsequently been lost (Milner and Larsen, 1991). The presence of these features provides a distinction between AMTL and agenesis or impaction. After narrowing the differential diagnosis of AMTL to pathology, accidental trauma, or intentional ablation, the presence of resorption and pathological indicators of the alveolar bone and concomitant oral pathology on adjacent dentition would indicate AMTL due to pathology. An absence of these would indicate tooth loss due to accidental trauma or intentional ablation. The presence of symmetry or an observed pattern in tooth loss, without associated dental and alveolar pathology, in multiple individuals within the same community, would indicate intentional ablation (Burnett and Irish, 2017a; Domett et al., 2013; Hrdliˇcka, 1940; Merbs, 1968; Stojanowski et al., 2016). Because intentional tooth ablation is usually associated with cultural values it is more commonly observed in the anterior dentition. Generally, molars are more affected by AMTL than the anterior teeth if the cause of the tooth exfoliation is not culturally induced. This is a result of the predisposition of the molar teeth to caries formation and severe attrition (Lukacs, 2007). Most studies that observe AMTL in archeological samples are typically associated with massive caries and/or severe macrowear with the subsequent exfoliation of the tooth (Costa, 1980; Hartnady and Rose, 1991; Lukacs, 2007; Molnar et al., 1983; Whittington, 1999). Severe periodontal disease will also result in the premature loss of a tooth. However, some researchers have asserted that periodontal disease does not usually result in exfoliation in prehistoric skeletal samples (Clarke and Hirsch, 1991). There has been no

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consistent pattern observed between the loss of the maxillary or mandibular dentition (Littleton and Frohlich, 1993; Lukacs, 2007).

Periodontal Disease Pathology Periodontal disease is initiated by polymicrobial plaque biofilm or abrasive effects of calculus (see “Dental Calculus” section), which are associated with the build-up of plaque (Clerehugh et al., 2013; Darveau et al., 2012; Hajishengallis et al., 2012). The build-up of plaque then causes an inflammatory response in the periodontal tissues of the teeth (Darveau, 2010). The inflammation agitates the periodontal connective tissues, which secures the tooth in the alveolar bone, manifesting as porosity, alveolar bone loss, and the development of pocketing or recessing, both vertical and horizontal, around the roots as the bone is resorbed. Vertical defects, or infrabony pockets, are, as the name suggests, characterized by vertical bone destruction and are defined where the pocket base is apical to the alveolar crest. Horizontal defects, or suprabony pockets, cause horizontal bone loss and are identified where the pocket base is coronal to the alveolar bone (Clerehugh et al., 2013). Periodontal disease sequentially affects the surrounding dentition, gradually exposing the roots and reducing support of the dentition, culminating in AMTL. Periodontal disease is cited as the most common cause of tooth loss in contemporary populations worldwide (Darveau, 2010) and once again females are more predisposed to periodontal infection (Armitage, 2013; Borgo et al., 2014; Pirie et al., 2007; Wu et al., 2015).

Paleopathology A range of methods for identifying and recording periodontal disease in skeletonized remains has been published. One of the most frequently seen approaches is the CEJ-AC, or cemento enamel junction to alveolar crest, method (e.g., Fyfe et al., 1993; Gargiulo et al., 1961; Khudaverdyan, 2010). The issue of intersample differences in “normal” CEJ-AC distances has led to the development of sample-specific correction factors when using this approach (e.g., Delgado-Darias et al., 2006; Tsilivakos et al., 2002), although problems with differential rates of attrition and unknown rates of continuous tooth eruption (see Clarke et al., 1986) are still serious drawbacks to such approaches. Another popular method, sometimes used in conjunction with the AC-CEJ method, is the use of Kerr’s (1988) categorization of the morphological changes to the interdental septa during periodontal disease (e.g., Oztunc et al., 2006; Wasterlain et al., 2011). Fig. 21.23 is an example of periodontal disease evidenced in the reactive alveolar bone and root exposure of

FIGURE 21.23 Molar root exposure and reactive alveolar bone suggestive of periodontal disease. Note calculus on the distolingual portion of the third molar (arrow). Left medial view of mandible (adult male from Canaveral, Florida, United States, NMNH 377439).

the left molars in an adult male from Canaveral, Florida, United States (NMNH 377439). Alveolar resorption has exposed a significant amount of the roots of the molars, resulting in very little support for the teeth. Rough porosity evidenced on the alveolar bone around the molar roots is indicative of an inflammatory response of the associated soft tissues.

INTERPRETING ORAL HEALTH Sex Differences in Oral Health There are clear and generally universal patterns in oral health based on biological sex. Meta-analysis using contemporary clinical data (Haugejorden, 1996), contemporary cultural data (Lukacs, 2011a), and prehistoric bioarcheological data (Lukacs and Thompson, 2008) have identified consistent sex differences in populations across many different cultures engaging in different subsistence economies. There has been a recent shift from the traditional behavioral dietary paradigm to a model that considers the pivotal role of female biology in the interpretation of oral health in bioarcheology (Ferraro and Vieira, 2010; Fields et al., 2009; Lukacs, 2008, 2011b, 2017; Lukacs and Largaespada, 2006; Watson et al., 2010; Willis and Oxenham, 2013). Such work has outlined the extensive literature pertaining to the clinical predisposition of females to poorer oral health, demonstrating their susceptibility as a consequence of sex-specific hormones, the size of salivary glands, the chemical composition of saliva and the confounding effects of pregnancy (Armitage, 2013; Borgo et al., 2014; Costa et al., 2017; Figuero et al., 2013; Jain and Kaur, 2015; Kamate et al., 2017; Mariotti and Mawhinney, 2013; Markou et al., 2009; Pirie et al., 2007; Rio et al., 2015; Silva de Araujo Figueiredo

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et al., 2017; Wu et al., 2015). It is clear that women are more susceptible to poorer oral health than males, a factor that needs to be taken into consideration when interpreting the prevalence of oral pathology in prehistoric assemblages.

Oral Health and Demographic Transitions Lukacs and Largaespada (2006: 550) emphasize the importance of context in a biocultural interpretation of the prevalence of caries during agricultural intensification. They predict that better oral health in pre-industrial hunter-gatherer groups, relative to farming communities, is correlated with the negative biological impacts on female health, particularly in the context of higher fertility and potentially more cariogenic diets in the latter. This observation has been developed by incorporating several different lines of evidence. The first is demographic shifts observed during the Neolithic demographic transition (NDT). The NDT defines a period where there was increased fertility in Neolithic communities, largely as a function of decreased birthing intervals in response to favorable environmental stimuli such as sedentism and sustainable agricultural crops (Bocquet-Appel and Naji, 2006). The effects of the NDT have been observed in prehistoric demographic data demonstrating an increase in birth rates (Bocquet-Appel and Naji, 2006; McFadden and Oxenham, 2018). The literature suggests a stable or declining birth rate in preagricultural groups, followed by a marked increase in fertility, subsequent to the transition to agriculture, which remained stable for 500 700 years, and then a leveling off or decline in birth rates, a pattern which has been demonstrated in many areas of the world (Bocquet-Appel and Naji, 2006; McFadden et al., 2018). The second is the variation in these demographic shifts as a function of the adoption of agriculture during the NDT. The data indicate that these demographic transitions observed through increases in fertility were slower at sites where agriculture was first being developed and more obvious in peripheral areas where the knowledge of agriculture spread (Bocquet-Appel and Naji, 2006), suggesting that population growth would be higher in populations peripheral to the origins of agriculture. It has been argued that sedentism may have been more of a catalyst than dietary change in reducing the birthing interval (BocquetAppel and Naji, 2006), however, Bellwood and Oxenham (2008: 22) suggest a consideration of both as significant in a “mutually reinforcing combination.” In a discussion of caries prevalence and fertility in relation to the NDT, Lukacs (2008) suggests the expression of a sex differentiation in caries frequency between males and females will follow the same trend as rises in fertility. This thesis has been supported for ancient Southeast Asia (Willis and Oxenham, 2013). Lukacs

(2008) further suggests that in geographical regions where agriculture was first being developed, the increase in the prevalence of caries would be small and insignificant, as a reflection of the gradual impact of changes in fertility, diet, and division of labor. While in the peripheral areas, where the transition to agriculture was faster and more intense, caries would temporarily increase at a distinct rate, the effect of increasing fertility concomitant with a decline in women’s oral health. There has been some reticence in interpreting sex differences in oral health as a function of fertility due to changes observed among both sexes. It should be reiterated that oral pathologies and the oral microbiome are complex, synergistic, and multifactorial, the underlying etiology and pathogenesis of oral pathology means both sexes are prone to developing them. The NDT, or indeed any other population-wide change, would impact the oral health of both sexes (Moynihan and Petersen, 2004; Petersen, 2003; World Health Organisation, 2003). The important difference is the increased vulnerability and biological susceptibility of females. The most parsimonious explanation for the higher frequencies of oral pathologies observed in communities influenced by the NDT with major changes in subsistence and demography is the correlation between fertility and female biology. As with all bioarcheological analyses, the interpretation of changes in oral pathology is context-specific. Situating the data and developing a multidisciplinary biocultural interpretative framework within the relevant context is imperative in understanding the environmental context, the demography of the assemblage, and any differences in diet or behavior to assist with the interpretations.

DENTAL CHEMISTRY Introduction Teeth form early in life (see “Dental Development” section), and the chemical analyses of primary dentin and enamel can provide information about the diet, health, and childhood residence of a person during the time of tooth formation (Katzenberg, 2008). Isotope and trace element analyses have become a ubiquitous aspect of modern bioarcheological research because they provide a direct means to address a diverse range of research questions that incorporate human diet, nutrition, subsistence strategies, mobility patterns, and sociocultural practices in the past (see reviews by Katzenberg, 2008; Lee-Thorp, 2008; Makarewicz and Sealy, 2015; Tsutaya and Yoneda, 2015; Turner and Livengood, 2017). The information gained from isotope and trace element analyses may be incorporated readily into any biocultural approach to

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understanding past people. Because the remains of the people themselves are being analyzed, these chemical methods may provide a direct understanding of how culture may have shaped biological responses, such as adaptation, and how it may have affected behavioral and wider societal changes that may have altered human biology, such as the impact of food choice on health. Specific chemical analyses can be chosen to tailor the research questions of each bioarcheological project and should be interpreted in conjunction with any available paleoenvironmental and archeological evidence, such as faunal and paleobotanical remains. The following subsections focus on the types of chemical analyses that are currently being used to address major research themes in the field: paleodietary reconstruction; breastfeeding and weaning; stress and disease; and human mobility; and places an emphasis on current trends and recently developed state-of-the-art methods.

Paleodietary Reconstruction: Bulk Stable Isotope Analysis Background Carbon stable isotope (δ13C) values are used to identify the consumption of plants with different photosynthetic pathways (C3, C4, CAM) and food sources from marine and terrestrial ecosystems (DeNiro and Epstein, 1978; Schoeninger and DeNiro, 1984; Smith and Epstein, 1971). Nitrogen and sulfur stable isotope ratios are used to assess marine, terrestrial, and freshwater food consumption patterns and, for δ15N values, the proportion of plants versus meat in the diet (DeNiro and Epstein, 1981; Schoeninger and DeNiro, 1984). Dietary amino acids are preferentially routed to synthesize proteinaceous tissues, of which bone collagen and tooth dentin are most commonly utilized for paleodietary reconstruction (Froehle et al., 2012). Both δ15N and δ34S values are representative of dietary protein because carbohydrates and lipids do not contain these elements (Ambrose, 1993; Richards et al., 2003). The δ13C values of enamel and apatite are representative of all the dietary macronutrients (proteins, carbohydrates, and lipids) (Krueger and Sullivan, 1984; Schwarcz and Schoeninger, 1991). Carbon from all three sources may also be utilized to synthesize bone collagen, but the preferential routing of amino acids for body proteins means that δ13C values are heavily representative of dietary protein (Froehle et al., 2010; Kellner and Schoeninger, 2007). Metabolic fractionation of stable isotope values, known as diet tissue spacing, occurs during tissue synthesis and must be corrected for when interpreting the human diet (Ambrose, 1993). Bone and dentin collagen δ13C values are about 5m higher and bone apatite and enamel 9 14m higher than diet (estimated to be near the lower range for

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humans) (for a review see Kohn and Cerling, 2002). There is a stepwise increase of 3 5m for δ15N values and 0 2m for δ13C values between trophic levels (Bocherens and Drucker, 2003; Hedges and Reynard, 2007). These trophic differences are used when comparing consumer and prey stable isotope values of bone collagen. One limitation of paleodietary studies is the variability in diet tissue spacing estimates, as they are not specific to humans and small changes in the spacing values may occur as a result of dietary (e.g., protein content), environmental, metabolic, or anthropogenic factors. This may significantly alter dietary interpretations, especially with regard to δ15N values (Makarewicz and Sealy, 2015). Comprehensive baseline dietary data are essential to correctly interpret human stable isotope data and are commonly established from analyzing the bone collagen of fauna from the site under investigation (but see discussion by Makarewicz and Sealy, 2015). Modern plant and animal values also may be used after correction for the Suess effect (the decrease in atmospheric δ13C values after the Industrial Revolution), but potential environmental variation between modern and prehistoric systems should be taken into consideration (Tieszen, 1991). The analysis of local baseline data can potentially address certain environmental factors that may affect dietary isotope values, such as the canopy effect (lower δ13C values in forest environments) (van der Merwe and Medina, 1989, 1991), the sea spray effect (high δ34S values of seawater affecting coastal terrestrial resources from sea spray) (Richards et al., 2003), aridity (high environmental δ15N values) (Heaton et al., 1986; Pate and Anson, 2008; Schwarcz et al., 1999), and manuring (higher δ15N values of manured plants) (Bogaard et al., 2007; Fraser et al., 2011; Styring et al., 2014). Baseline dietary data are a fundamental resource for interpreting human stable dietary isotope values and mixing models have been developed to estimate the proportion of certain foods within the diet (reviewed by Phillips et al., 2014). The use of mixing models incorporating Bayesian modeling methods has become increasingly popular, as this approach allows for the input of multiple dietary sources with variable element concentrations while addressing diet tissue spacing variation (Erhardt and Bedrick, 2013; Gordo´n et al., 2017; Hopkins and Ferguson, 2012; Parnell et al., 2010). However, mixing models cannot account for the complexities of metabolic routing (e.g., Webb et al., 2017), and correct interpretations rely on the researcher providing the full range of isotope variation for the complex food webs of humans in the past, which may overlap considerably (Phillips et al., 2014). Thus, mixing models may be best suited as exploratory tools to provoke new lines of thinking about diet and subsistence strategies in the past (Makarewicz and Sealy, 2015).

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Bone collagen and dentin can be affected by taphonomic processes, and quality indicators have been developed (%C, %N, %S, C:N, C:S, N:S, and collagen yield) to assess diagenetic alteration (Ambrose, 1990; Nehlich and Richards, 2009; van Klinken, 1999). There are also nondestructive methods, such as Raman spectroscopy, that are used to assess if the collagen is well preserved in a sample before destruction for stable isotope analysis (King et al., 2011). Bone apatite is subject to diagenetic alteration and therefore the biogenic δ13C values of the mineral portion of bone may not be a true representative of dietary values (Lee-Thorp and Sponheimer, 2003; LeeThorp, 2008), although a number of screening processes have been applied to address this issue such as Fourier transform infrared spectroscopy (FTIR), SEM coupled with EDX, X-ray diffraction, and microscopic observations (optical, SEM, TEM) (King et al., 2011; Lee-Thorp and Sponheimer, 2003; Reiche et al., 2003; Webb et al., 2014). Enamel is more mineralized than bone, and therefore more resistant to diagenetic alteration in the burial environment (Elliot, 1994; Kohn and Cerling, 2002; LeeThorp and Sponheimer, 2003).

Paleodietary Reconstruction: Bulk Stable Isotope Analysis in Bioarcheological Research The analysis of carbon (δ13C), nitrogen (δ15N) and, more recently, sulfur (δ34S) stable isotope ratios of prehistoric human tissues is a well-established method for reconstructing the diets of past people (see reviews by Hedges et al., 2005; Katzenberg, 2008; Lee-Thorp, 2008; Makarewicz and Sealy, 2015) (see also “Dental Calculus” section). Used in conjunction with paleopathological approaches, chemical analyses can provide important information about health, nutritional status, and mortality (Huss-Ashmore et al., 1982; Reitsema, 2013; Reitsema et al., 2016). Inadequate nutrition may result in diseases such as rickets, scurvy, and iron-deficiency anemia, compromise the immune response, and cause physiological and psychological stress (see Chapter 16). The physiological response of these processes may be observable in the skeleton in the form of disrupted growth, bony lesions, and nonspecific indicators of stress such as LEH (see “Disturbances in Dental Development” section, above) and cribra orbitalia (Larsen, 2015; Roberts and Manchester, 2005). The first point of contact for any food or drink is the oral cavity. Oral health indicators such as caries, calculus, and periodontal disease have multifactorial etiologies (see Identifying Dental Wear and Oral Disease section). Combining oral health information with the results of chemical analyses may provide insight into the possible

influence of diet on the development of these conditions (Bonsall and Pickard, 2015; Kinaston et al., 2016; Tomczyk et al., 2013; Turner, 2015). Chemical analyses may also be used to identify possible cultural and social practices and their corresponding impacts on the lives of prehistoric and historic communities, leading to a more comprehensive understanding of health and wellbeing in the past (Cheung et al., 2017; Dent, 2017; Kinaston et al., 2013a; Knudson and Stojanowski, 2008; Knudson et al., 2015; Quinn and Beck, 2016; Reitsema and Vercellotti, 2012; Turner et al., 2012).

Paleodietary Reconstruction: CompoundSpecific Isotope Analysis Background Proteins are composed of 20 amino acids, 11 of which are termed “nonessential” and may be synthesized by the body through a process known as transamination and 9 are “essential” and must be obtained from the diet (Barrett, 2012). Essential amino acids are rarely transaminated (only during excretion), because they are directly absorbed from the diet, whereas nonessential amino acids may undergo multiple transamination processes during synthesis, transformation, and excretion (Jim et al., 2006; Macko et al., 1987). Nonessential amino acids can be synthesized by higher organisms and may be representative of multiple macronutrient carbon sources (lipid, protein, and carbohydrate), whereas essential amino acids must be obtained from dietary protein (Howland et al., 2003; Jim et al., 2006). The δ15N values from bulk stable isotope analysis represent the dietary values and the sum of all fractionations of amino acids within the collagen sample, but the δ15N value of each amino acid is dependent on its specific level of isotopic enrichment of 15N during biochemical processes (O’Connell, 2017).

Paleodietary Reconstruction: CompoundSpecific Isotope Analysis in Bioarcheological Research In recent years, compound-specific isotope analyses (CSIAs) of individual organic compounds in bone, such as amino acids and lipids, have been developed as a tool for paleodietary reconstruction (Corr et al., 2008; Fogel and Tuross, 2003; Jim et al., 2004; Naito et al., 2016; Webb et al., 2015). The comparison of δ15N values of “source” and “trophic” amino acids can provide information about trophic position and has been used to address aquatic food consumption in the past (e.g., Naito et al., 2010, 2013, 2016). This is because the “source” amino acids undergo only slight fractionation, whereas the “trophic” amino acids undergo an observable enrichment in

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N with each trophic step (Chikaraishi et al., 2014; O’Connell, 2017; Styring et al., 2010). Carbon stable isotope values of specific amino acids are representative of the source of carbon in the diet (mainly from primary producers within an ecosystem) because of how the body utilizes essential and nonessential amino acids (Jim et al., 2006). The comparison of δ13C values from specific essential and nonessential amino acids therefore can provide information regarding protein and whole-diet carbon sources (e.g., aquatic and terrestrial foods) and C3/C4 resources (Corr et al., 2005, 2008; Fogel and Tuross, 2003; Webb et al., 2015). It should be noted that more research is required to understand the metabolism of source carbon for nonessential amino acids (Makarewicz and Sealy, 2015). The δ13C values from CSIAs of bone lipids, including cholesterol, have been used to assess the carbon sources of all dietary macronutrients, but the method is still in its infancy (Howland et al., 2003; Jim et al., 2004; Stott et al., 1999). CSIAs typically require smaller sample sizes than bulk isotope analyses, but the necessity to separate the compounds before isotopic analysis increases the analytical time and cost. However, as there are more analyses being conducted on one sample, CSIA can potentially provide more information than bulk isotope analyses. It is beneficial to analyze all amino acids, even if they are not being used for the current research, because it allows for the potential future use of the isotope values of these compounds.

Paleodietary Reconstruction: Trace Elements Background During life, trace elements such as strontium (Sr), barium (Br), and lead (Pb) may replace calcium in the inorganic component (hydroxyapatite) of bone and enamel (see review by Burton, 2008). These trace elements enter the food chain from the biosphere through primary producers such as plants. There is a successive decrease in Sr/ Ca and Ba/Sr ratios with increasing trophic levels because of the process of biopurification (Burton et al., 1999; Elias et al., 1982). Differences in Sr/Ca and Ba/Ca ratios are observed throughout food webs and, for the latter, between different ecosystems: marine and terrestrial (see reviews by Burton and Price, 2002; Lee-Thorp and Sponheimer, 2006). However, variability of strontium and barium concentrations has also been observed within trophic levels and between related species within an ecosystem (Lee-Thorp and Sponheimer, 2006). Marine systems generally display lower Ba/Ca ratios compared with terrestrial systems (Arnay-de-la-Rosa et al., 2009; Burton and Price, 1990; Shaw et al., 2011). Lead is found in nonpolluted environments at many orders of magnitude lower than strontium and barium (Burton, 2008). Exposure to

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anthropogenic sources of lead (at levels as low as one partper-billion) can cause major health effects and neurological development problems in infants and children (Humphrey, 2016).

Paleodietary Reconstruction: Trace Elements in Bioarcheological Research Strontium and barium were the first elements used for trace element analysis for paleodietary reconstruction due to the correlation between a reduction of strontium and barium with increasing positions in the food chain (Price et al., 1985). It was assumed that the relative proportion of plants and meat in a consumer’s diet could be ascertained using these trace elements (Sr/Ca and Br/Ca) (e.g., Burton and Price, 1990; Price and Kavanagh, 1982; Sillen, 1981). However, issues with the early methods became apparent because the strontium in bone is not just a reflection of dietary strontium, but is associated with mean dietary Sr/Ca and, similarly, bone barium is associated with dietary Br/Ca (Burton, 2008). Quantitative interpretations of plant vs. meat foods from trace element analysis have been critiqued because the Sr/Ca and Ba/Sr ratios of multicomponent diets will reflect the foods with the highest mineral components, which may lead to the overestimation of certain foods, especially those with high calcium components (Burton, 2008; Burton and Price, 2002; Burton and Wright, 1995). Concentrations of Sr and Ba and Sr/Ca have been used to address questions surrounding the consumption of plant and animal products, including milk in the past (Lugli et al., 2017; Schutkowski et al., 1999). Trace element analysis, especially Sr/Ca and Ba/Ca, of teeth is gaining popularity to address breastfeeding and weaning practices and childhood diet in the past (discussed in the following section). Differences in environmental strontium and barium abundances have been found between regions with varying geologies and climates, leading some researchers to use these trace elements as a marker of human mobility (Burton et al., 2003; Cucina et al., 2011; Knudson et al., 2012). Higher concentrations of lead in teeth and variation in lead isotope values are used to assess potential lead exposure and migration (see review by Humphrey, 2016). Other trace elements, such as copper (Cu), zinc (Zn), and magnesium (Mg) have interested researchers as paleodietary markers (Arora et al., 2014; Jaouen et al., 2017; Safont et al., 1998; Schutkowski et al., 1999). However, the applications are still developing (Dolphin et al., 2005; Ezzo, 1994a, b; Jaouen et al., 2017; Martin et al., 2015) and space constraints limit the current discussion of these methods. Diagenetic alteration of bone apatite affecting biogenic trace element concentrations is a major issue and

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must be taken into account for any such study (Dudgeon et al., 2016; Fabig and Herrmann, 2002; Lee-Thorp and Sponheimer, 2003; Reynard and Balter, 2014; Sillen, 1989). There are a number of methods to assess bone diagenesis (see Bulk Stable Isotope Analysis Background section), none of which can quantify the amount of contaminated bone or the effect it may have on biogenic trace elements (Burton, 2008). As previously mentioned, enamel is extremely robust in the burial environment and therefore retains the biogenic trace element values from the time of tooth formation.

Patterns of Breastfeeding and Weaning: Background The use of stable isotope analysis to identify breastfeeding relies on the fact that a nursing infant is one trophic level (step in the food chain) higher than its mother, as it is consuming her tissue in the form of breast milk (Fogel et al., 1989). As a result, the δ15N and δ13C values of an infant’s proteinaceous tissues that were formed during the time of breastfeeding are elevated compared to its mother’s tissues by B2 4m and B1 2m, respectively (Fuller et al., 2006a; Jenkins et al., 2001). Variation from the expected δ15N values of young infants has been observed and attributed to a number of possibilities, including maternal and infant stress (see Understanding Stress and Disease From Chemical Analyses section) and gut biome metabolism (Beaumont et al., 2015; Kinaston et al., 2009; Reynard and Tuross, 2015). Oxygen stable isotopes ratios are primarily a reflection of those in drinking water. There is a stepwise enrichment in δ18O values from drinking water to breast milk and, as breast milk is the primary source of water for infants, this trophic increase is observable in the δ18O values of their forming tooth enamel (Wright and Schwarcz, 1998).

Patterns of Breastfeeding and Weaning: The Bioarcheological Research Breastfeeding and weaning practices are integral to examining child health, and are issues that are paramount to infant and child survival rates (Humphrey, 2010; Lewis, 2007). Stable isotope, and more recently trace element analysis, have been used to identify breastfeeding practices, the timing of weaning, and types of supplementary foods consumed by young individuals (see reviews by Dean, 2017; Humphrey, 2016; Jay, 2009; Mays, 2013; Smith and Tafforeau, 2008; Tsutaya and Yoneda, 2015). Traditionally, researchers have determined the average δ15N value of the adult female bone collagen in a skeletal assemblage and then compared this to infant and young child δ15N values to assess the duration of breastfeeding,

the timing of weaning, and childhood diet in past populations (e.g., Fuller et al., 2006a; Jay et al., 2008; Prowse et al., 2008; Richards et al., 2002). Recently, researchers have introduced the use of Bayesian modeling to help refine interpretations of breastfeeding and weaning by accounting for variability in a sample caused by such factors as the unknown rate of bone remodeling and modeling in children (de Armas et al., 2017; Tsutaya et al., 2016b; Tsutaya and Yoneda, 2013). Stable isotope analysis of high-resolution incremental sections of dentin and targeted areas of dentin is becoming a popular method to provide more nuanced information regarding breastfeeding, weaning, childhood diet, and stress (Beaumont et al., 2013b, 2014; Guiry et al., 2016; Henderson et al., 2014; King et al., 2017; van der Sluis et al., 2015). This method allows for the dietary reconstruction of the people who survived the vulnerable earlier life stages (i.e., the adults) and for the determination of sex and age differences in diet during childhood (Beaumont et al., 2013a; Eerkens and Bartelink, 2013; Henderson et al., 2014; Kinaston and Buckley, 2017). Oxygen, and to a lesser extent carbon, stable isotope analysis of sequential samples of tooth enamel have also been used to investigate patterns of breastfeeding and weaning in the past (Dupras and Schwarcz, 2001; Wright and Schwarcz, 1998, 1999). Time-resolution stable isotope data from intratooth sequential sampling should be interpreted carefully because of uncertainties surrounding enamel formation times (see Dental Development section) (Balasse, 2003). The use of barium, strontium, and calcium trace elements in tooth enamel has recently been developed to address breastfeeding and weaning patterns (introduced above). Mapping changes in the concentration in these elements in incremental sections of tooth enamel can identify the trophic shift of breastfeeding and differences between the mineral component of supplementary food and breast milk on a nuanced scale in humans, other primates, and hominins (Austin et al., 2013; Humphrey et al., 2008). Stable strontium isotope ratios (δ88/86Sr) and calcium stable isotope ratios (δ44/42Ca) recently have been used to address trophic shifts in diet, and are a possible method to address childhood diet and the duration of breastfeeding in the past (Knudson et al., 2010; Lewis et al., 2017; Tacail et al., 2017).

Understanding Stress and Disease From Chemical Analyses: Background Nutritional stress can lead to a negative nitrogen balance and raise δ15N values as the body catabolizes its own tissues (Fuller et al., 2005; Hobson et al., 1993; Katzenberg, 2012; Mekota et al., 2006). Other physiological changes,

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such as pregnancy, can also affect δ15N values (Fuller et al., 2004). Variations in both δ15N and δ13C values have been observed between nonpathological and pathological bone (Katzenberg and Lovell, 1999; Olsen et al., 2014).

Understanding Stress and Disease From Chemical Analyses: The Bioarcheological Research Research has shed light on the potential influence of physiological stress and diseases on bone collagen and tooth dentin stable isotope values, although the magnitude of the stable isotope changes is variable and requires further research (Reitsema, 2013). Comparisons of the δ15N values of high-resolution incremental sections of dentin from individuals who survived childhood and those who did not have found elevated values in the latter and attributed this to possible physiological stress (Beaumont et al., 2015). A number of studies have observed fetal and perinatal individuals that display elevated δ15N values compared to the adult female mean (Fuller et al., 2006b; Nitsch et al., 2011; Richards et al., 2002), and some have attributed this to possible maternal and fetal stress (Beaumont et al., 2013b; Beaumont et al., 2015; Kinaston and Buckley, 2017; Kinaston et al., 2009). The comparison of tooth δ15N and δ13C values, representative of childhood diet and physiology, and bone δ15N and δ13C values, representative of the diet/physiology nearer to the time of death (B10 years for adult femoral cortical bone; Hedges et al., 2007), can help researchers understand the dietary “life history” of an individual (Davis and Pineda-Munoz, 2016; Eriksson and Lide´n, 2013; Mays et al., 2017; Reitsema and Vercellotti, 2012; Salamon et al., 2008; Sealy et al., 1995; Tsutaya et al., 2016a; Turner et al., 2012). This is known as a life course approach (Agarwal, 2016). Comparisons of diet from specific life stages of the “survivors” and “non-survivors” can be undertaken with isotope analyses, leading to more comprehensive interpretations that address selective mortality within the context of the Osteological Paradox (DeWitte and Stojanowski, 2015; Reitsema et al., 2016; Sandberg et al., 2014).

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forms soil, releases minerals in underground aquifers and mixes with atmospheric inputs and precipitation. The strontium sources obtainable within an ecosystem constitute the bioavailable 87Sr/86Sr values that enter food webs through primary produces such as plants (Hartman and Richards, 2014; Price et al., 2002). Seawater displays a 87 Sr/86Sr ratio of 0.7092 and soils and plants in coastal areas affected by sea spray may display elevated 87Sr/86Sr ratios closer to that of seawater (Bentley et al., 2007). Strontium substitutes for calcium in apatite, and it was hypothesized that the 87Sr/86Sr of enamel was representative of the 87Sr/86Sr ratio of the diet during the time of tooth formation (with little fractionation). A recent controlled feeding experiment has confirmed this, further validating the use of 87Sr/86Sr in paleomobility studies (Lewis et al., 2017). The δ18O values of the inorganic hydroxyapatite of tooth enamel reflect the local drinking water, and are therefore representative of the δ18O values of the local precipitation and nearby rivers, streams, and springs (Luz et al., 1984). Global precipitation δ18O values are primarily influenced by prevailing weather patterns and are closely linked to both altitude and latitude (Bowen and Wilkinson, 2002; Dansgaard, 1964). There are variations in δ18O values as a result of seasonal weather patterns, but the δ18O values of tooth enamel will represent an annual average during the time of tooth mineralization, taking into account the fractionation between skeletal tissue and environmental water (Lee-Thorp, 2008). Variation can also result from other factors such as humidity, temperature, perspiration, breast milk consumption, and distance from the sea (Dupras and Schwarcz, 2001; Gat, 1996; White et al., 2000). Researchers typically develop environmental baseline data from modern plant, animal, water, and soil samples, and prehistoric fauna to determine the isotopic variation in the local and mid-range environment (Burton and Price, 2013; Evans et al., 2009, 2010; Evans and Tatham, 2004; Price et al., 2002). The adequacy of baseline data to represent the range of isotopic diversity in local biomes and the regional landscape has been questioned, and there is a move toward developing more comprehensive isoscapes that incorporate spatial, environmental, and temporal factors through predictive modeling, including GIS (Emery et al., 2017; Pellegrini et al., 2016).

Human Mobility and Migration: Background Strontium isotope ratios (87Sr/86Sr) in human tooth enamel are representative of the place of childhood residency (Lee-Thorp, 2008). The underlying geology dictates the 87Sr/86Sr of the soils, plants, and animals in the area from which a person obtained their food during the time of tooth formation (Bentley, 2006; Knudson and Price, 2006). As bedrock weathers and breaks down, it

Human Mobility and Migration: The Bioarcheological Research Strontium (87Sr/86Sr) and oxygen (δ18O) isotope analyses are commonly used to address human mobility patterns, which can provide an insight into social relationships, methods of food acquisition, and addressing boundaries

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delineated by political agendas (see reviews by Budd et al., 2004; Lee-Thorp, 2008; Price et al., 2002; Slovak and Paytan, 2011). The δ18O values and 87Sr/86Sr ratio of tooth enamel remain unchanged throughout life. If a person moves to an area with a different underlying geology and bioavailable 87Sr/86Sr or environmental δ18O values, the isotopic signatures within their enamel will be different from the “local” people in the burial population, thus identifying them as “non-local” (Bentley et al., 2004; Price et al., 2002; Wright, 2005). The use of multiple types of biogeochemical analyses can potentially help refine interpretations of geographical origins (Gregoricka et al., 2017; Kinaston et al., 2013b; Knudson and Price, 2006; Mu¨ldner et al., 2011; Turner et al., 2012). Research focusing on δ18O and δD (hydrogen stable isotope values) of organic tissue, including bone collagen and tooth dentin has begun (Kirsanow et al., 2008; Koon and Tuross, 2013; Reynard and Hedges, 2008; Topalov et al., 2013) but space constraints limit the discussion of this new research avenue. Sulfur stable isotope analysis also has been used to identify nonlocal individuals who may have moved from coastal areas and were buried in inland cemeteries. As discussed above, coastal terrestrial ecosystems, marine foods, and some freshwater organisms display high δ34S values, and the presence of an outlier in a burial population with “marine” δ34S values may be indicative of human movement from the coast (Hemer et al., 2017; Vika, 2009).

DENTAL CALCULUS Pathology: Dental Calculus Formation Dental calculus is calcified bacterial plaque that forms throughout an individual’s life on the subgingival and/or supragingival tooth surfaces (see Periodontal Disease section) underneath a layer of nonmineralized plaque (Hillson, 1996). Plaque consists of bacteria and amorphous fluids, and dental calculus forms as a result of the deposition of calcium phosphate crystals into this plaque (Lieverse, 1999). The boundary between dental calculus and enamel or dentin is strong. There is bonding and sometimes complete fusion between the calculus and tooth apatite or enamel crystals (Rohanizadeh and Legeros, 2005), and residue may remain adhering to the teeth even after cleaning. Dental calculus is mostly inorganic, consisting primarily of calcium and phosphorus, with minor components of carbonate, sodium, magnesium, silicon, iron, and fluoride, and the minerals brushite, whitlockite, octacalcium phosphate, and hydroxyapatite (Hayashizaki et al., 2008; Lieverse, 1999; White, 1997). There is also an organic component (approximately 15% 20%) to calculus, consisting of microparticles (previously called microfossils) such as

phytoliths and starch granules, as well as biomolecules such as proteins, glycoproteins, lipids, DNA, carbohydrates, and bacteria (Lieverse, 1999; Warinner et al., 2014a,b). The microparticles and biomolecules in dental calculus originate from anything that comes in contact with the mouth, including food, animal and plant fibers, lithic detritus, bacteria, parasites, protein, and DNA (Radini et al., 2017; Warinner et al., 2014b). The rate of calculus formation, its microscopic structure, and how organic components are incorporated within it, are highly variable between individuals depending on diet, genetics, the bacterial microenvironment of the mouth (including pH and salivary flow), and dental care (Hanihara et al., 1994; Lieverse, 1999; White, 1997). However, the effects of each of these components regarding the formation of dental calculus are not well understood. There is some research suggesting that relatively high alkaline conditions created by a high-protein diet may be associated with an increased calculus build-up; however, sugary or high-carbohydrate foods also have been linked to an increase in deposits (Hillson, 2005; Lieverse, 1999). Differences in the oral fluids of individuals may be more important for determining if one is more prone to calculus formation. The unpredictable variability of dental calculus formation and composition recently was shown in an empirical study of the plant foods eaten by modern Twe foragerhorticulturalists living on the Namibia Angola border (Leonard et al., 2015). Several of the plants in the Twe diet produce microparticles (both phytoliths and starch granules), but the study found that even when people were eating microparticle-producing plants, the microparticles did not necessarily appear in dental calculus. Leonard et al. (2015) were able to confirm that microparticles extracted from dental calculus are only useful for identifying the presence or absence of plant foods and plant processing in the mouth, but not the proportion they contribute to the diet. Both the modern microparticle study (Leonard et al., 2015), and to a lesser extent the stable isotope studies described below (Poulson et al., 2013; Salazar-Garcı´a et al., 2014; Scott and Poulson, 2012), have successfully shown that analysis of various components of dental calculus are a useful way to look at population-level dietary trends, but not the diet of specific individuals.

Paleopathology: Microparticle Analyses of Dental Calculus in Bioarcheology Analysis of calculus can provide information on ancient health, diet, and environment without harming the teeth (Kelley and Larsen, 1991; Klepinger et al., 1977; Lieverse, 1999). Dental calculus first gained the attention of archeologists in the 1970s, but it took over 30 years for researchers

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FIGURE 21.24 An SEM image of archeological dental calculus. Note the irregularity of the layers as well as the “enveloping” characteristics.

to realize the full potential of this calcified bacterial microfilm. The first phytolith studies were focused on modern and archeological ungulate (cattle, sheep, and horse) dental calculus (Armitage, 1975; Dobney and Brothwell, 1987; Dobney, 1994; Dobney and Brothwell, 1986, 1988) and such work introduced recording standards still used by most researchers today (Dobney and Brothwell, 1987). Microparticle analyses have been the most common bioarcheological studies of dental calculus and the majority of this research has been used to study the plant component of diets. There are a few classes of microparticles that are commonly found in dental calculus and studied regularly: biogenic silica (phytoliths and diatoms) and starch granules. A wide range of other identifiable and unidentifiable microparticles, such as pollen and spores, unsilicified plant tissues, fungal spores, bacteria, charcoal, insects, pseudoparasites, and animal hairs have also been identified. The analysis of nondietary microremains, such as fibers and fungus, has since become the focus of a few researchers (e.g., Afonso-Vargas et al., 2015; Blatt et al., 2011; Hardy et al., 2015; Radini et al., 2016), and has been thoroughly summarized by Radini et al. (2017). After death, the lamellar, rigid, and enveloping character of dental calculus provides a relatively stable and pristine environment protected from many taphonomic processes

that commonly affect cementum or dentin. Fig. 21.24 shows an SEM image of archeological dental calculus where the irregularity of the layers, as well as the “enveloping” characteristics, can be seen. Typically, bioarcheologists focus on removing and analyzing the visible supragingival calculus build-up that creates a band on or, in extreme cases, a cap over the tooth. A simple scoring method to grade calculus deposits as mild, moderate, or severe developed by Dobney and Brothwell (1987) is commonly used in bioarcheological research (Hillson, 2008). Fig. 21.25 shows “moderate” to “severe” grades of calculus build-up on multiple maxillary teeth from a prehistoric adult individual from the c.6700-year-old Con Co Ngua, Vietnam, site. There have been attempts to rinse teeth that have barely visible or invisible deposits in order to recover any microparticles that may be embedded in thin layers resulting from a new calculus deposit forming just prior to death, or from deposits that were removed either during life or after death (Boyadjian et al., 2007). However, concern has been raised about the damage the brief (5 minutes) and weak (4% HCl) acid wash had on the morphology of the teeth and microscopic features in the enamel. It was suggested acid washes should be done only after conducting a detailed microwear analysis (Boyadjian et al., 2007; Kucera et al., 2011). Other

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FIGURE 21.25 An image of calculus deposits on multiple maxillary teeth from a skeleton from the Con Co Ngua, Vietnam site (Brothwell, 1981; grades 2 3).

studies have shown this outer layer of enamel can hold dietary evidence in the form of grass, hair, and asteriform (or globular echinate) phytoliths embedded at the end of microscopic scratches on the enamel (Lalueza Fox and Perz-Perez, 1994). A detailed SEM analysis of teeth with ephemeral or no visible calculus is warranted prior to destructive acid washes. The oldest example of microparticles extracted from a hominin are from a 2-million-year-old fossil of Australopithecus sediba (Henry et al., 2012). Analyses of Neanderthal dental calculus have expanded what we know about the role of plants in their diet and health (Hardy et al., 2012; Henry et al., 2011, 2014; SalazarGarcı´a et al., 2013). Each of these studies identified several starch granules that displayed features consistent with heat damage from cooking. These data refute previous assertions that Neanderthals ate an almost exclusively protein rich diet, which was thought to have contributed to their ultimate demise (Henry et al., 2011, 2014). At sites where both Neanderthal and modern human dental calculus were examined, it appears there were no significant differences in the breadth of their plant diets (Henry et al., 2014). In addition to Neanderthals, studies of modern human European dental calculus have also given an insight into diet, showing the use of cereals, legumes, tubers, and

fungus in various populations, as well as evidence of probable cooking techniques (e.g., Blondiaux and Charlier, 2008; Hardy et al., 2009; Henry et al., 2014; Juhola et al., 2014; Lalueza Fox et al., 1996; Lazzati et al., 2015; Power et al., 2015; Warinner et al., 2014a). There have been a few studies of microparticles extracted from the Near East (Hardy, 2007; Hardy et al., 2009) and the Middle East (Cummings et al., 2016; Henry and Piperno, 2008; Walshaw, 1999) that show the importance not only of cultivated cereals, but also wild foods in the diet. Similar results are seen further east in China, where four recent dental calculus studies focus on starch granule analysis (Li et al., 2010; Tao et al., 2015; Wang et al., 2015; Zhang et al., 2017) and show the use of various cereals, underground storage organs (USOs), acorns, palm, and beans. A study of pre-Columbian Caribbean dental calculus similarly demonstrates a diverse diet throughout the region, including maize and both wild and cultivated USOs and legumes (Mickleburgh and Paga´n-Jime´nez, 2012). Central (Scott Cummings and Magennis, 1997) and South American (Piperno and Dillehay, 2008; Wesolowski et al., 2010) dental calculus studies show regional and temporal differences in plant consumption. In Oceania, dental calculus studies have addressed questions of water availability (Dudgeon and Tromp, 2012) and the importance of the sweet potato in the diet (Tromp, 2012; Tromp and Dudgeon, 2015), as well as the stability of plant resources through time (Horrocks et al., 2014; Tromp, 2016).

Paleopathology: Chemical Analyses of Dental Calculus for Bioarcheological Research The high variability of the contents of dental calculus between individuals has made bulk chemical analyses difficult to interpret (see also Dental Chemistry section), but have been attempted by a few research groups (Eerkens et al., 2014; Poulson et al., 2013; Salazar-Garcı´a et al., 2014; Scott and Poulson, 2012). For the most part, these studies seem to disregard the high variability of dental calculus between individuals and even between different teeth of the same individual, which make it extremely difficult to create quality control criteria around C:N ratios for dental calculus, as is standard practice for other stable isotope studies (e.g., DeNiro et al., 1985). Two additional methods of chemical analysis have been utilized to study the contents of dental calculus: FTIR and thermal desorption/pyrolysis gas chromatography mass spectrometry (TD/Py-GC-MS). FTIR appears to be able to distinguish between starch and material that is comprised of similar long-chain glucoses, such as cellulose, and may be used in the attempt to taxonomically identify specific starch granules (Horrocks et al., 2014).

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FTIR analysis proved to be difficult, as samples must be dry and exposed, so cannot be in a mounting medium or obscured with a cover slip. This finding suggests that to analyze potential starch granules, samples need to either be rinsed off the slide, where there is a potential to lose the specific granules you want to target, or another subsample of dental calculus can be used. However, due to the unpredictable nature of dental calculus formation, the likelihood of finding a similar granule is low. With methodological refinement, this technique could prove quite useful in future microparticle studies where starch granules are degraded. The third major method used for chemical analysis of dental calculus is TD/Py-GC-MS, which allows for the identification of both free or unbound and bound or polymeric organic components (including lipids) (Buckley et al., 2014). Like FTIR, this method targets individual components within the dental calculus. This method has been applied to dental calculus from Neanderthals (Hardy et al., 2012), an early hominin (Hardy et al., 2015), and several Sudanese individuals (Buckley et al., 2014). The analyses have shown evidence of potential smoke inhalation (Buckley et al., 2014; Hardy et al., 2012) and possibly the use of yarrow and chamomile; a finding interpreted by the authors as medicinal use of these plants (Hardy et al., 2012).

Paleopathology: aDNA and Protein Analyses of Dental Calculus for Bioarcheological Research Biomolecular techniques are rapidly developing and, recently, three major studies have demonstrated the utility of analyzing aDNA (Adler et al., 2013; Warinner et al., 2014b; Weyrich et al., 2017) and proteins (Warinner et al., 2014a) extracted from dental calculus. Oral bacteria, the major component of dental calculus, are the primary target of aDNA calculus studies. Changes in the oral microbiota have reflected the shift from agriculture to industrialization (Adler et al., 2013) and aDNA analyses also hint at the potential to identify markers of cardiovascular and respiratory disease, and dietary components (Warinner et al., 2014b; Weyrich et al., 2017). Additionally, human mitogenomes have been extracted from the dental calculus of six 700-year-old North American individuals, despite human DNA being less than 1% of the total DNA recovered from the dental calculus after enrichment (Ozga et al., 2016). Although this needs to be explored in further regions and time periods, this study opens up exciting new possibilities for aDNA and paleopathological analyses that do not destroy human remains.

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Proteomic analyses of dental calculus are also used to better understand ancient oral pathologies and diet. One major benefit of protein analysis is the identification of both pathological bacteria and human innate immune system proteins (Warinner et al., 2014b). There is also potential for species-specific dietary proteins to be recovered. For example, human dental calculus has shown areas in Europe and Eurasia where species-specific milk was consumed up to 5000 years ago, as well as an absence of milk consumption in historic Central West Africa; confirming indirect assumptions as well as previously unidentified variability in European milk consumption (Warinner et al., 2014a). This most recent methodological advancement is likely to enable identification of many more dietary markers within dental calculus (Hendy et al., 2018).

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