Exploring oral paleopathology in the Central Andes: A review

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Exploring oral paleopathology in the Central Andes: A review Celeste Marie Gagnon Wagner College, 1 Campus Rd, Staten Island, NY 10301, United States

A R T I C LE I N FO

A B S T R A C T

Keywords: Andes Dental caries Macrowear Alveolar abscess Periodontal disease Calculus

This targeted review of oral paleopathology in the Central Andes explores research that focuses on a set of interrelated, multifactorial processes: dental caries, macrowear, alveolar abscess, antemortem tooth loss (AMTL), periodontal disease, and the presence of dental calculus. These conditions help characterize oral health because they result from the culturally mediated interaction of individuals’ oral cavity with their external environment. To better understand how osteologists working in the Central Andes have interpreted the frequencies of these conditions, I review the etiology of each, as well as discuss the important issues in their analyses. I then highlight studies that integrate of a number of oral paleopathological conditions, that examine associations between oral conditions and other skeletal indicators of health, or that use multivariate statistical techniques to analyze conditions. In the Central Andes, these proxies for oral health have generally focused on several key research themes including the introduction of domesticated foods may have occurred earlier than expected, but that populations may have maintained mixed subsistence strategies for a significant period. Researchers have also identified that changes accompanying Inca imperialism were likely not as detrimental to local populations as was Spanish colonialism. Finally, the long-practiced, culturally important, activity of chewing coca has been shown to create an identifiable pattern of oral paleopathological conditions.

1. Introduction Oral paleopathological conditions are among the most commonly collected osteological data, as teeth often preserve well in archaeological contexts. There a number of oral paleopathological conditions, but this review examines a limited set of interrelated, multifactorial processes: dental caries, macrowear, alveolar abscess, antemortem tooth loss (AMTL), periodontal disease, and the presence of dental calculus. These processes are considered pathological because they can negatively impact the function of the oral cavity, as well as the overall health of individuals (Hillson, 1996; Larsen, 2015). The presence and extent of these conditions can help researchers characterize past human biocultural experiences because they result from the culturally mediated interaction of an individual’s oral cavity with their external environment. Additionally, data collection methods for these macroscopically observable conditions, are relatively straightforward (excepting dental calculus) (Alt et al., 2012; Hillson, 1996; Kelley Mark and Larsen, 1991; Larsen, 2015; Roberts and Manchester, 2007). As Verano (1997) noted in his influential review of Andean paleopathological research, frequencies of oral paleopathological conditions, particularly dental caries, are often included as one of a variety of health and dietary indicators used to reconstruct community-level behavior (e.g. Benfer, 1990; Buzon et al., 2012; Hubbe et al., 2012;

Juengst et al., 2017a, 2017a,b; Juengst and Skidmore, 2016; Klaus et al., 2010; Lowman et al., 2018; Oliveira and Neves, 2015; Turner, 1978; Verano and Rossen, 2011). Since his review, researchers have come to recognize that simple percentages of individuals or teeth affected by oral paleopathological conditions do not capture the complex risk factors for developing these conditions. Of particular concern is the age-progressive nature of oral conditions. At issue are both the cumulative nature of insults to teeth across an individual’s the life course, as well as variations in the period of exposure of different tooth types that results from the dental eruption sequence. Additionally, the past 20 years has seen a dramatic increase in bioarchaeological research the Andes, integrating archaeological and biological data to increase our knowledge of the lived experiences of Central Andean people, as well as providing a number of new methodological approaches to interpreting these conditions. In this review, I offer a discussion of our current understanding of a specific set of oral paleopathological conditions. A large number of studies of Central Andean skeletal samples include the analysis of these conditions as a part of their research design. However, the focus of this review is studies in which oral paleopathological conditions are the primary data set, because it is in these studies that the complexities of risk factors are most fully addressed. Such studies have investigated shifts from foraging to food production and from mixed subsistence strategies to

E-mail address: [email protected]. https://doi.org/10.1016/j.ijpp.2019.10.003 Received 6 February 2019; Received in revised form 18 October 2019; Accepted 22 October 2019 1879-9817/ © 2019 Elsevier Inc. All rights reserved.

Please cite this article as: Celeste Marie Gagnon, International Journal of Paleopathology, https://doi.org/10.1016/j.ijpp.2019.10.003

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2.2. Macrowear

agricultural intensification, analyzed the effects of imperial expansion, and documented coca chewing. Based on this review, I offer suggestions for methodological approaches and future research directions.

Macrowear is the loss of enamel or dentin on the occlusal surfaces of teeth caused by the friction of mastication resulting from either attrition (tooth on tooth contact) or abrasion (tooth with object contact) (Hillson, 1996; Kaidonis, 2008; Powell, 1985). Thus, macrowear is often used as a proxy for understanding dietary composition. For example, the decreasing bite force characteristic of the shift from tough to softer foods decreases macrowear (Constantino et al., 2010; Kaidonis, 2008). This relationship suggests that less macrowear at the population level can indicate a transition from foraging to farming or an intensified use of domesticates (Deter, 2009; Littleton and Frohlich, 1993; Sciulli, 1997). Differences in the mechanics of chewing tough versus soft foods affects the form of macrowear, particularly on the posterior teeth, so that foragers tend to have even wear across tooth surfaces (Fig. 2), while agriculturalists’ teeth tend to wear angularly (Fig. 3) (Deter, 2009; Larsen, 2015; Molnar, 1971; Smith, 1984). Macrowear can also be increased by the presence of particles in foods (e.g. sand), which increases abrasion (Chattah and Smith, 2006; Lucas et al., 2013). Attrition and abrasion can remove bacterial plaque from tooth surfaces (Lukacs, 1989) and worn teeth have significantly less topography (Powell, 1985), both of which can decrease the risk of dental caries. Wear on anterior teeth can also tell us about human diet. Among Pre-Hispanic, Brazilian individuals, Turner and Machado (1983) identified macrowear affecting the lingual surfaces of maxillary anterior teeth (LSAMAT). They suggested that this pattern was the result of using the maxillary anterior teeth and tongue to process tubers. LSAMAT has also been identified among living Hadza women who use their anterior maxillary teeth to peel the coarse skin from tubers (Berbesque et al., 2012), supporting Turner and Machado's (1983) hypothesis.

2. Oral paleopathological conditions The six conditions discussed in this review affect both teeth and their supporting structures. Teeth are unique in the human body because the portion that interacts directly with the environment is composed of inorganic enamel; insults to this tissue cannot heal and thus accumulate throughout a person’s life course (Hillson, 1996; Larsen, 2015). Additionally, the tooth eruption sequence results in significantly different periods of exposure for different teeth, resulting in variability of risk by tooth type. Finally, variation in exogenous risk factors from dietary practices and other oral behaviors create yet more complexity in outcomes. To better understand how the six conditions are interrelated, how they are influenced by endogenous and exogenous factors, and how they have been used to explore the lives of Central Andean peoples, I first offer a brief discussion of each condition.

2.1. Dental caries Dental caries (Fig. 1) is the most commonly reported oral paleopathological condition in the osteological literature (Table 1). Its etiology is complex, but diet is an essential factor in the process (Hillson, 2008). Carious lesions, the result of dental caries, are areas of localized destruction caused by the acidic by-products of bacterial fermentation of sugars (Hillson, 1996; Ortner and Putschar, 1981); therefore, diets high in simple sugars or carbohydrates are cariogenic because they provide food for bacteria (Brudevold et al., 1988; Burt and Ismail, 1986; Cucina et al., 2011; Goodman et al., 1984; Larsen, 2015; Larsen et al., 1991; Mundroff-Shrestha et al., 1994; Zero, 2004). The presence of sugars and gelatinized starches in the mouth results in increased colonization of dental plaque by Streptococcus mutans, S. sobrinus, and Lactobacillus spp. (van Houte, 1994). The presence of these bacteria also decreases dental plaque pH, which further promotes the reproduction of cariogenic bacteria while suppressing cariostatic bacteria (Lingström et al., 2000; van Houte, 1994). This dysbiosis (i.e., microbial imbalance) creates a positive feedback system that promotes the formation of dental cavities. Dental caries is also affected by tooth type, including eruption timing and variations in morphology (Hillson, 2008; Larsen, 2015), as well as the composition of saliva and its level of flow, as it can buffer the oral environment and harden enamel (Laine, 2002; Lukacs, 2008; Salvolini et al., 1998).

2.3. Alveolar abscess If allowed to progress, dental caries and macrowear can expose living pulpal tissue to the oral environment, leading to pulpitis and pulp death (Clarke and Hirsch, 1991; Hillson, 1996). Infections of the pulp allow bacteria, their waste, and the cellular products of inflammation to travel through the apical foramen into the periapical tissues (Waldron, 2008), forming a periapical granuloma, often referred to as an abscess. Sufficient pus may accumulate in the granuloma to initialize marginal bone resorption and allow for drainage into the soft tissue, creating a true abscess (Fig. 4) (Dias and Tayles, 1997; Hillson, 1996; Roberts and Manchester, 2007; Waldron, 2008). Whether caused by untreated dental caries or severe macrowear, an advancing alveolar abscess compromises the integrity of the bone and periodontal ligament, potentially leading to AMTL (Fig. 1) (Ortner and Putschar, 1981). 2.4. Periodontal disease Periodontal disease is an inflammatory process that causes loss of alveolar connective tissue and bony structures (Gosman, 2012; Hillson, 1996). Periodontal disease can be caused by mechanical (Ortner and Putschar, 1981) or chemical irritation (Indriati and Buikstra, 2001; Langsjoen, 1996), as well as dysbiosis of oral bacteria inhabiting dental plaque. This dysbiosis is indicated by a shift in bacterial communities from those characterized by a balance of Streptococcus and Antinomies spp. to plaque dominated by Actinomyces (Socransky, 1977; Williams, 1990) and red complex bacterial species (i.e., Porphyromonas gingivalis, Tannerella forsythia, and Treponema denticola) (Rôças et al., 2001). The presence of these bacteria initiate immune and inflammatory responses that compromise periodontal tissues. As a result of periodontal disease, alveolar bone becomes porotic and the margin sharp and ragged (Fig. 5), leading to compromised bony and ligamentous tooth support and ultimately AMTL (Gosman, 2012; Hillson, 1996).

Fig. 1. Superior view of mandible showing advanced caries affecting right 1st and 2nd molars, and antemortem loss of all molars on the left side and the 1st molar on the right side. 2

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Table 1 Central Andean studies discussed in text, key issue explored, and oral paleopathological conditions examined. Map ID

Author’s/Year

Issue explored

Dental caries

3 1 1 3 6&8 7 7 5, 6 & 10 4 5 9 1 2 5 7

Haas and Llave (2015) Watson et al. (2010) Watson et al. (2013) Watson and Haas (2017) Pezo-Lanfranco and Eggers (2010) Lambert et al. (2012) Gagnon and Wiesen (2013) Pezo-Lanfranco et al. (2017) Turner (2015) Williams and Murphy (2013) Klaus and Tam (2009) Langsjoen (1996) Indriati and Buikstra (2001) Murphy and Boza (2012) Gagnon et al. (2013)

foraging to farming foraging to farming foraging to farming foraging to farming agricultural intensification agricultural intensification agricultural intensification agricultural intensification supra-local systems supra-local systems supra-local systems coca chewing coca chewing coca chewing coca chewing

X X X X X X X X X X X X X X

Macrowear

Alveolar abscess

X X X X X X X X

AMTL

Periodontal disease

Dental calculus

X X

X X X X X

X X X X X X X X X X

X

X X

X

X

Fig. 2. Medial view of right mandible showing flat wear characteristic of foragers.

Fig. 4. Lateral view of right mandible showing abscess of 1st molar.

Fig. 3. Superior view of mandible showing angled wear characteristic of agriculturalists.

2.5. Calculus Dental plaque, if not mechanically removed, interacts with salivary mineral ions and becomes calcified into calculus (Fig. 6) (Hillson, 1996; Lieverse, 1999; Lukacs, 1989; Radini et al., 2017; White, 1997). A variety of dietary and non-dietary factors affect this calcification, including the composition of the oral microbiome, the nature of saliva, and oral pH; therefore, the presence or amount of calculus is not indicative of particular diets. However, a wide variety of items that were present in the oral cavity during life can accumulate in calculus (Radini et al., 2017), including micro-plant fossils (e.g., phytoliths, pollen, starch granules) that, when extracted, can be used to identify what

Fig. 5. Lateral view of the left maxilla showing periodontal disease affecting the alveolar bone of the 1st through 3rd molars.

plants were eaten or processed in the mouth (Fox and Perez-Perez, 1994; Gagnon et al., 2013; Radini et al., 2017; Reinhard et al., 2001). Dental calculus has also been shown to preserves the DNA of the oral 3

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through the use of multivariate statistical techniques, such as principle factor analysis and General Estimating Equations, which allow several factors and their interactions to be examined simultaneously, while preserving sample size. The studies of Central Andean past populations highlighted below take into account these complexities. Each of the published studies explores more than one condition (Table 1), and many employ multivariate statistical techniques in order to address issues of sample heterogeneity and variability. 3. Oral paleopathology in the Central Andes Andean bioarchaeologists often use oral paleopathological conditions to reconstruct diet. At the site level, diet has been strongly linked to ecological and economic systems, and as such, its reconstruction can provide insight into political economy, sociopolitical complexity, and human adaptive regimes. Specifically, researchers have documented the transitions from foraging to farming, from mixed to intensive agricultural systems, and from local to supra-local political systems. Bioarrchaeologists have also focused on identifying coca chewing and the role it played in sociopolitical and ritual life.

Fig. 6. Lateral view of right maxilla showing calculus deposits affecting all teeth.

microbiome (Adler et al., 2013; De La Fuente et al., 2013; Warinner et al., 2015). The reconstruction of the oral microbiome from calculus holds the potential to aid in dietary reconstruction and the differential diagnosis of oral conditions. This is because the particular bacterial constituents of dental plaque depend on the diet and oral biology and infectious oral conditions such as dental caries, alveolar abscess and periodontal disease are linked to shifts in the community of oral bacteria (Costalonga and Herzberg, 2014). Diversity and balance in the oral microbiotic community is essential for human health (Zarco et al., 2012); for example, dysbiosis has been linked to cardiovascular disease and diabetes (Cullinan and Seymour, 2013; Dewhirst et al., 2010; Slocum et al., 2016). Therefore, the reconstruction of oral microbiomes from calculus might allow paleopathologists to track systemic diseases not otherwise recorded in human skeletal tissues.

3.1. Foraging to farming Given the close relationship among dental caries, macrowear, and dietary composition, the analysis of oral conditions has been used across the globe to chart the transition from foraging to food production (Cohen and Armelagos, 1984; Eshed et al., 2010; Kelley Mark and Larsen, 1991; Lillie and Richards, 2000; Littleton and Frohlich, 1993; Pechenkina et al., 2002; Temple and Larsen, 2007; Turner, 1979; Willis and Oxenham, 2013). Although the Andes are a primary center of domestication (Pearsall, 2008; Piperno and Dillehay, 2008; Piperno, 2011), few researchers have used oral health data to explore the transition to farming economies in this area, in part because of the limited number of collection available. Working in the Titicaca Basin (Fig. 7, Table 2), Watson and Haas (2017) examined dental macrowear with the goal of understanding Middle to Late Archaic (6000 – 4700 BC) dietary transitions (Table 3). Previously, Haas and Llave (2015) observed extreme macrowear on individuals recovered from the site of Soro Mik’aya Patjxa. This pattern, coupled with the recovery of a number of sandstone grinding tools, led them to suggest that the population extensively used wild seeds as a food source. Watson and Haas (2017) completed a more detailed analysis of macrowear in a sample of these individuals by quantifying the occlusal changes in each tooth using a standard 10-point wear scale, calculating a second molar to first molar ratio (M2/M1) for each individual, and characterizing the angle of wear using an M1buccal/ M2lingual ratio, which takes advantage of the six year difference in the eruption of M1 and M2. Data were analyzed using principal factor analysis, a multivariate statistical technique that can compare groups that have differing age structures (Watson et al., 2010). Watson and colleagues (Watson et al., 2013; Watson and Haas, 2017) identified a pattern of relatively flat wear and a low frequency of dental caries that commonly characterizes foraging groups. In addition, they identified LSAMAT in three individuals, suggesting that tubers were also part of the diet. Future analysis of starch recovered from dental calculus may confirm that the seeds and tubers included in the group’s diet were the wild progenitors of later important domesticates, highlighting the Titicaca Basin as an important location for domestication of Andean crops. Watson and co-authors (Watson et al., 2013, 2010) also used oral health indicators to track spatial and temporal differences in diet from the Initial Period (IP) through Early Intermediate Period (EIP) (Table 3) in the Lower Azapa valley of Chilé (Fig. 7, Table 2). Archaeological data suggested that during this time (1500 BC – AD 500) coastal residents were marine foragers while inland groups relied on a mixed subsistence strategy. They reconstructed diet by calculating both the number of

2.6. Analyzing oral paleopathological conditions Given the diverse but interrelated etiologies of the oral paleopathological conditions discussed above, it stands to reason that simple frequencies of any one condition may not be able to be interpreted in a meaningful way. For example, the multiple pathways to AMTL suggest that dental caries, macrowear and periodontal disease frequencies must be considered together when interpreting the significance of AMTL. Additionally, the cumulative effects of oral paleopathological conditions mean that variations in the ages-at-death within a population and in the tooth types represented among study individuals can lead to biased or spurious results. Many statistical techniques, such as chi square and Fisher’s exact used to test for significant differences in oral condition frequency, assume that observations are independent. However, it is common to make comparisons of condition frequencies by pooling all observable teeth or alveoli from individuals representing a particular period or cultural group (Turner, 1979). These pooled samples may therefore include from one to 32 different observations from each individual and as a result, not all observations within each comparative sample are independent. Because of variability in preservation and archaeological recovery, the number and types of teeth that can be observed for each individual are also often highly variable. Given that posterior teeth are more likely to be preserved and are at greater risk for dental caries, these differences can introduce significant bias into analyses. For example, a well-preserved skeletal sample might include a large number of complete dentitions, but a poorly-preserved sample to which it might be compared, may contain mostly posterior teeth that would artificially raise the carious lesion frequency of the poorly preserved sample relative to the well-preserved sample. To address these biases, multiple conditions should be considered simultaneously, and analyses must include age-at-death and sex estimations, political economic organization, and other cultural and ecological factors that influence lived experience. This work is best done 4

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Fig. 7. Map of the Central Andes, identifying archaeological sites discussed in text. See Table 1 for citations, Table 2 for locations and Table 3 for temporal associations.

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Table 2 Map identifications, regions and locations of sites discussed. Map ID

Region

Location

Site

1 1 1 2 2 2 2 3 3 4 5 5 5 6 6 7 7 7 8 9 9 10

Southern Coast Southern Coast Southern Coast Southern Coast Southern Coast Southern Coast Southern Coast Southern Highlands Southern Highlands Southern Highlands Central Coast Central Coast Central Coast Central Coast Central Coast North Coast North Coast North Coast North Coast North Coast North Coast Northern Highlands

Azapa Valley Azapa Valley Azapa Valley Moquegua Valley Moquegua Valley Moquegua Valley Moquegua Valley Titicaca basin Titicaca basin Urubamaba Valley Rímac Valley Rímac Valley Rímac Valley Huaura Valley Huaura Valley Moche Valley Moche Valley Moche Valley Jequetepeque Valley Lambayeque Valley Lambayeque Valley Marañón Valley

Author’s/ Year

Chiribaya Alta Chen-Chen Yaral Algondal Soro Mik'aya Patjxa Soro Mik'aya Patjxa Machu Picchu Puruchuco-Huaquerones Armatambo Puruchuco-Huaquerones Los Pinos Los Pinos Cerro Oreja Cerro Oreja Cerro Oreja Puémape Morrópe Laguna de los Condores

Watson et al. (2010) Watson et al. (2013) Langsjoen (1996) Indriati and Buikstra (2001) Indriati and Buikstra (2001) Indriati and Buikstra (2001) Indriati and Buikstra (2001) Haas and Llave (2015) Watson and Haas (2017) Turner (2015) Williams and Murphy (2013) Pezo-Lanfranco et al. (2017) Murphy and Boza (2012) Pezo-Lanfranco and Eggers (2010) Pezo-Lanfranco et al. (2017) Gagnon et al. (2013) Lambert et al. (2012) Gagnon and Wiesen (2013) Pezo-Lanfranco and Eggers (2010) Klaus and Tam (2009) Klaus and Tam (2009) Pezo-Lanfranco et al. (2017)

have occurred earlier than previously identified using traditional archaeological methods (Piperno and Dillehay, 2008; Verano and Rossen, 2011).

affected individuals by group and the number of affected teeth by group of dental caries and AMTL using general linear modeling to identify significant differences (Table 1). They also employed principal factor analysis to document differences in occlusal wear, as well as M2/M1 and M1buccal/M2lingual ratios. Watson and colleagues expected coastal foragers to be characterized by lower dental caries frequencies, greater wear rates, and flatter wear planes compare to inland groups. Furthermore, they anticipated increases in the frequency of dental caries and decreases in the degree of macrowear through time as the use of agricultural products intensified. The data did not, however, support these expectations, but suggested that both coastal and inland groups engaged in mixed subsistence strategies throughout the period. The analyses of Watson and colleagues highlight the fact that the level and form of macrowear and frequency of carious lesions together can be used to track the introduction of domesticated plants to the diet. These data suggest that the shift from foraging to food production may

3.2. Agricultural intensification Although the transition to food production in the Central Andes has not been well studied using oral paleopathological conditions, the development of intensive agricultural systems has been a greater focus. Archaeological data show that important domesticates, including fruits, maize, and manioc, came into use during the IP, and that by the Late Intermediate Period (LIP) agricultural systems were significantly intensified such that field crops became an essential item of production (Piperno and Dillehay 2008; Pearsall, 2008). To better understand the timing and context of this intensification, researchers have examined dental caries in combination with other conditions.

Table 3 Period/Horizon associations dates, and map identifications of sites discussed. Map ID

Period/Horizon

Site/s

Date

Author’s/Year

1 3 3 8 1 1 7 7 7 2 2 2 2 9 10 1 6 6 5 10 4 5 5 9

Archaic Archaic Archaic Initial – Early Intermediate Period Initial – Early Intermediate Period Initial – Early Intermediate Period Early Intermediate Period Early Intermediate Period Early Intermediate Period Middle Horizon – Late Intermediate Middle Horizon – Late Intermediate Middle Horizon – Late Intermediate Middle Horizon – Late Intermediate Middle Horizon – Late Intermediate Middle Horizon – Late Intermediate Late Intermediate Period Late Intermediate Period Late Intermediate Period Late Intermediate Period Late Horizon Late Horizon – Colonial Late Horizon – Colonial Late Horizon – Colonial Colonial

sites not named in study Soro Mik'aya Patjxa Soro Mik'aya Patjxa Puémape sites not named in study sites not named in study Cerro Oreja Cerro Oreja Cerro Oreja Chiribaya Alta Chen-Chen Yaral Algodonal sites not named in study Laguna de los Condores sites not named in study Los Pinos Los Pinos Armatambo Laguna de los Condores Machu Picchu Puruchuco-Huaquerones Puruchuco-Huaquerones Morrópe

7000 – 2000 BC 6000 – 4700 BC 6000 – 4700 BC 1800 – 1 BC 1500 BC – AD 500 1500 BC – AD 500 400 BC – AD 200 400 BC – AD 200 400 BC – AD 200 AD 800 – 1350 AD 800 – 1350 AD 800 – 1350 AD 800 – 1350 AD 900 – 1475 AD 800 – 1470 AD 1000 – 1250 AD 1000 – 1300 AD 1000 – 1300 AD 1300 – 1470 AD 1470 – 1532 AD 1438 – 1570 AD 1470 – 1540 AD 1470 – 1540 AD 1536 – 1750

Langsjoen (1996) Haas and Llave (2015) Watson and Haas (2017) Pezo-Lanfranco and Eggers (2010) Watson et al. (2010) Watson et al. (2013) Gagnon et al. (2013) Lambert et al. (2012) Gagnon and Wiesen (2013) Indriati and Buikstra (2001) Indriati and Buikstra (2001) Indriati and Buikstra (2001) Indriati and Buikstra (2001) Klaus and Tam (2009) Pezo-Lanfranco et al. (2017) Langsjoen (1996) Pezo-Lanfranco et al. (2017) Pezo-Lanfranco and Eggers (2010) Pezo-Lanfranco et al. (2017) Pezo-Lanfranco et al. (2017) Turner (2015) Williams and Murphy (2013) Murphy and Boza (2012) Klaus and Tam (2009)

Period Period Period Period Period Period

6

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caries associated with increased maize consumption was only significant among females. This pattern suggests that the negative effects of maize intensification on oral health were concentrated among women. In the Moche valley, the development of gender inequality in access to food resources was part of the processes that led to the development of a political economy based on intensive maize production during the EIP. The work of Pezo-Lanfranco (Pezo-Lanfranco and Eggers, 2010; Pezo-Lanfranco et al., 2017) and Gagnon and colleagues (Gagnon and Wiesen, 2013; Lambert et al., 2012) adds to our understanding of agricultural intensification in the Central Andes. Although the archaeological data indicate that domesticates were produced during the IP, the osteological data suggest that significant changes in the lived experience of northern and central coastal peoples occurred later in the EIP, a pattern that continued into the MH and LIP. This lag between early agricultural production and the negative health consequences of its intensification was made visible through the integration of multiple oral paleopathological conditions and the use of multivariate statistical techniques.

Working in the north and central coasts of Peru, Pezo-Lanfranco and Eggers (2010) investigated the transition from the mixed subsistence systems to intensive agriculture using the frequency of carious lesions and AMTL (Table 1). They analyzed dental remains dating from the IP through early EIP (1800 – 1 BC) at Puémape in the Jequetepeque valley, and from the LIP (AD 1000–1300) at Los Pinos in the Huaura valley (Fig. 7, Tables 2 and 3). Archaeological investigations at Puémape indicate that IP occupants were fisher-gatherers with some access to maize, but they fully intensified their subsistence regime by the LIP. Pezo-Lanfranco and Eggers hypothesized there would be a steady increase in the frequency of both dental caries and AMTL resulting from caries during the EIP as a result of this shift. Carious lesions were separately categorized as affecting only enamel, dentin, or pulp, as well as if they were located on occlusal or non-occlusal surfaces. Teeth were pooled by period, and frequencies of carious lesions and AMTL were compared using univariate statistical techniques, methods that cannot account for differences in age structure among samples nor in tooth type representation. Contrary to the authors’ expectations, the shift in subsistence from the IP to the EIP at Puémape was not associated with a significant temporal increase in the frequency of dental caries or AMTL, but both conditions were more common in the LIP sample from Los Pinos. Building on their previous research, Pezo-Lanfranco et al. (2017) compared oral paleopathological conditions among the LIP central coast residents of Los Pinos and Armatambo in the Rímac valley, as well as to Middle Horizon (MH) through LIP (AD 800–1470) and Late Horizon (LH) (AD 1470–1532) individuals from Laguna de los Cóndores in the northern highlands (Fig. 7, Tables 2 and 3). They examined a wide variety of oral conditions (Table 1), but again explored temporal and spatial variation through univariate statistics. Given the documented ecological, economic, and cultural differences between coastal and highland groups, the authors hypothesized that highland populations would be characterized by better oral health. They found that, indeed, highland teeth were less often affected by oral paleopathological conditions, indicating that central coastal diets were more cariogenic and abrasive than highland diets, regardless of period. These data suggest that, although wear can mediate the formation of dental caries as previously noted, this relationship does not remove the risk of caries formation among agriculturalists. With a more focused look at the EIP, Lambert et al. (2012) investigated agricultural intensification on the north coast by combining bone and enamel δ13Capatite values with oral pathological condition data (Table 1). Analyzing remains from Cerro Oreja in the Moche valley (Fig. 7, Tables 2 and 3), they found that δ13Capatite values indicated a dramatic increase in the consumption of C4 resources from the early to middle EIP. This shift was accompanied by a significant increase in the frequency of dental caries, alveolar abscesses, and AMTL. These data suggest that on the north coast, agricultural intensification, particularly of maize, began during the middle EIP. To further characterize this change, 173 individuals from Cerro Oreja were examined by Gagnon and Wiesen (2013) for the degree of macrowear in addition to the frequency of dental carious lesions, alveolar abscesses, and AMTL. The General Estimating Equations (GEE) method, a semiparametric, multivariate technique often employed in epidemiological research, was used to examine the simultaneous and interactive effects of individuals’ age-at-death, sex, and cultural period phase on frequencies of oral pathological conditions. Additionally, they employed a repeated subject strategy, which accounts for the correlation among measures of different teeth within individuals. Model estimates of population parameters are calculated using individual teeth, allowing the largest possible sample size, but the teeth of an individual remain linked, allowing standard errors to be adjusted for the correlation among the teeth of each individual, thus addressing the problem of variability in tooth type representation. Gagnon and Wiesen (2013) were therefore able to clarify the pattern identified by Lambert et al. (2012), noting that the temporal increase in the frequency of dental

3.3. Supra-local systems: Inca and Spanish imperialism The LH and Colonial Periods represented transformational eras in the Central Andes as supra-local political structures developed through the incorporation of multiple regions into Inca and then Spanish Empires (Moseley, 2001). Several researchers have integrated a number of oral paleopathological conditions with other bioarchaeological data to explore the effects of these shifts on Central Andean communities. Turner (2015) examined gendered patterns in diet among 70 ‘servants’ of the Inca who lived at Machu Picchu in the Peruvian southern highlands during the LH (AD 1438–1570) (Fig. 7, Tables 2 and 3). Previous isotopic analyses of strontium, lead, and oxygen suggested that these servants migrated to Machu Picchu from across the empire, post-adolescence. To chart the relationship between oral paleopathological conditions and dietary carbon (δ13C) and nitrogen (δ15N) values, Turner calculated individual-level mean macrowear scores, as well as frequencies of carious lesions, alveolar abscesses, and AMTL, thus avoiding the issue of variation in tooth type representation and the statistical problems caused by pooling teeth. Pearson’s correlation coefficient was calculated to test for significant associations between oral pathological conditions and stable isotopic values. The frequency of carious lesions among young males showed no association with particular stable isotopic values, suggesting that diet was not the only factor affecting their oral health. In contrast, a significant association between carious lesions and stable isotopic values among younger females suggests that caries formation was influenced by low protein consumption. Furthermore, dental caries and macrowear affecting the premolars of young females may indicate their involvement in masticating maize for chicha (corn beer) production. Among older females, dental caries was strongly influenced by their diet after their arrival in Machu Picchu. Williams and Murphy (2013) investigated the effects of Inca imperialism on the central Peruvian coast by tracking patterns in diet and health among LH (AD 1470–1540) occupants of Puruchuco-Huaquerones in the Rímac valley (Fig. 7, Tables 2 and 3). Ethnohistorical data suggest that the area was peacefully incorporated into the Inca Empire, and so Williams and Murphy hypothesized that the local population would have experienced few negative impacts. They analyzed stable isotopes as well as a variety of osteological and oral paleopathological (Table 1) conditions. They characterized oral conditions by calculating both the number of individuals and the number of teeth affected. To address the problem of tooth type representation, separate anterior and posterior caries frequencies were calculated. Additionally, individuals were compared by age group to account for the age-progressive nature of oral conditions. Among the sample of 90 individuals, little significant variation was found. The integration of stable isotopic and oral 7

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and maintenance of various types of social and ritual relationships in the Central Andes (Allen, 1981, 1988; Isbell, 1978; Julien, 1988; Murra, 1986; Netherly, 1988; Weismantel, 1988) since at least 6000 BC (Dillehay et al., 2010). Given the cultural importance of coca, understanding the paleopathology of coca chewing has been a significant area of interest. For example, coca chewers add cal (an alkali) to the leaves to activate the alkaloids that are absorbed by the oral mucosa. Klepinger et al. (1977) posited that the use of cal with coca increased the formation of dental calculus; however Ubelaker and Stothert (2006) demonstrated that cal used in chewing is not incorporated into dental calculus, so calculus presence is not indicative of coca use. Researchers were able to identify metabolites of coca in the hair of mummies recovered from Atacama region of northern Chile (7000 – 1500 BC) and the Moquegua valley in southern Peru (1000 BC – AD 1500) (Aufderheide et al., 1994; Cartmell et al., 1991; Rivera et al., 2005). Building on this research, Langsjoen (1996) and Indriati and Buikstra (2001) analyzed the oral health of these individuals in an attempt to identify a pattern of oral conditions indicative of coca chewing (Fig. 7, Tables 2 and 3). Langsjoen (1996) found a significant increase in the frequency of posterior AMTL among Chilean mummies from groups that also tested positive for metabolites. He noted an increased presence of periodontal disease and carious lesions at the CEJ (rather than on the crown) in coca chewing groups as well. Although cal does not promote calculus deposits, its caustic nature irritates the gingiva, leading to periodontal disease, exposure of tooth roots, and development of root caries. Chewers develop a specific pattern of alveolar bone loss and root (not crown) caries in the region of their mouth where they habitually hold their quid (Fig. 8). Further defining the effects of coca chewing, Indriati and Buikstra (2001) created a scale of strong, mild, and weak dental indicators of chewing (Table 1). The strongest indicator of coca chewing included the exposure of severe mandibular roots with affected teeth displaying root cavities. Less clear indications of coca chewing include maxillary molars that are affected by root exposure and caries, and affected premolars when adjacent molars have been lost antemortem. All individuals who Indriati and Buikstra identified as definite or probable users on the basis of oral health, also tested positive for coca alkaloids (Cartmell et al., 1991). Applying Indriati and Buikstra's (2001) method, Murphy and Boza (2012) examined coca chewing in the LH community of PuruchucoHuaquerones in the Rímac valley of the Peruvian central coast (Fig. 7, Tables 2 and 3). Ethnohistoric and ethnographic records identify coca as an important resource controlled by the Inca elite. Although archaeological data suggest that Puruchuco-Huaquerones may have been involved in Inca administration of the region, Murphy and Boza found no status differences in coca use in their sample. Additionally, they documented lower frequencies of coca chewing compared to frequencies identified in southern Peru and northern Chile. This finding suggests that coca was either less available or not used in the same way on the Peruvian central coast as on the southern coast. Further north, Gagnon and colleagues (2013) also analyzed oral paleopathology to trace the political uses of coca in the Moche valley. As a result of taphonomic factors, they were unable to score root caries, so they examined contrasting patterns of periodontal disease, crown caries, and AMTL using General Estimating Equations, as well as documenting the presence of coca microfossils in dental calculus (Table 1). Examining the EIP occupation of Cerro Oreja (Fig. 7 and Tables 2 and 3), they investigated a shift in access of costal groups to coca produced on the western slopes of the northern Andes. They found that as highland groups increased their presence on the coast, use of coca decreased among Cerro Oreja’s residents. As highlanders retreated or were driven from the western foothills, coca use again increased, but only among males. It appears that sociopolitical changes resulting from the retaking of the area by coastal groups reshaped social rituals and gender relations. Coca chewing is an ancient and widespread Central Andean

Fig. 8. Lateral view of right mandible showing conditions consistent with coca chewing: carious lesions of the buccal CEJ of the 1st through 3rd molars, and periodontal disease affecting the alveolar bone of the 1st molar.

paleopathological conditions suggests that males may have had diets slightly enriched in protein compared to females. Comparisons of their paleopathological data with a number of other central coast LH sites and a north coast Colonial Period site support their hypothesis that there was little negative impact on the quality of the diet as a result of Inca control. To better understand Spanish colonialism in the Lambayeque valley of north costal Peru, Klaus and Tam (2009) examined the dental remains of 378 individuals for the full suite of oral paleopathological conditions (Table 1). Pre-Hispanic remains recovered from ten sites dating to the MH and LIP (AD 900–1475) were compared to Colonial period remains excavated from the site of Mórrope (AD 1536–1750) (Fig. 7, Tables 2 and 3). Individuals were divided into six age classes to attempt to address the age-progressive nature of oral paleopathological conditions, and data were subject to G-test, a univariate statistical technique. Klaus and Tam identified a significant pattern of increase in the frequency of dental caries, particularly among women, as well as elevated AMTL and calculus deposition among the Colonial period group. They suggest that these changes represent a shift toward a highstarch, lower-nutrient diet resulting from social and economic transformations made by the Spanish. On the north coast of Peru, highquality land and irrigation water were taken over by the Spanish for sugar production, and native residents were forcibly relocated to less productive land, while still being required to pay tribute. Additionally, the shift from camelids to European livestock and the commodification of meat disrupted traditional access to protein resources. These changes limited the diversity and quality of the diet. The brunt of these economic changes affected women, patterns that were also observed during the EIP in the Moche Valley (Gagnon and Wiesen, 2013). Studies of supra-local systems benefit from the integration of oral paleopathological data with other biological data at both the individual (Turner, 2015; Williams and Murphy, 2013) and group levels (Klaus and Tam, 2009). In these studies, a variety of methods were used to address the issue of tooth type representation and the age-progressive nature of oral health conditions. Earlier forms of Andean imperialism such as Wari and Tiwanaku of the MH and Chimú of the ILP have not been examined through the primary use of oral paleopathological conditions, but the studies of later expressions presented herein, suggest that the lived experience of incorporation into a supra-local political system are variable. Inca imperialism appears to have had less of a negative oral health impact than did Spanish colonialism.

3.4. Coca chewing Ethnographic and ethnohistorical research indicates that the chewing of coca leaf is and has been an essential element in the creation 8

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creates an identifiable pattern of oral paleopathological conditions. This pattern must be considered when interpreting oral health indictors because it provides us a way to asses if access to and use of coca was part of changing sociopolitical conditions. Notably, the work highlighted here focuses on Peru, leaving much yet to be explored other regions of the Central Andes. Finally, although the focus of this target review has been the Central Andes, the work beyond coca chewing speaks to other regions of the world. Research suggests that because dental caries, macrowear, alveolar abscess, AMTL, periodontal disease, and the presence of dental calculus have complex, multifactorial, and interrelated etiologies, these conditions hold the greatest potential for addressing questions about diet and behavior when analyzed together. As the studies highlighted above indicate, patterns in oral paleopathology have significant power for characterizing lived experience and social change when these data are combined with other osteological datasets (e.g., demography, stable isotopic signatures, skeletal paleopathological conditions) as well as with archaeological data. It is through an examination of the interaction of these variables that researchers in the Central Andes and beyond, can most clearly link oral health to sociocultural characteristics and thus begin to compare and contrast the lived experience of past peoples.

practice. Given the impact of chewing on patterns of periodontal disease, carious lesions, and AMTL, it is essential that the possible role of coca chewing in shaping oral paleopathology be considered. Analyses of coca chewing have identified significant variation in the extensiveness of the practice as well as its sociocultural dimensions (Gagnon et al., 2013; Murphy and Boza, 2012). This work cautions us to examine each population for indications of coca use as well as differences within and between communities as part of any analysis of oral paleopathology. 4. Conclusions This targeted review explores how the analysis of some oral paleopathological conditions has advanced since Veranoös (1997) review of paleopathology in the Andes, highlights a number of important trends in the analysis of these conditions, and suggests a number of future directions, including increased use of multivariate statistical techniques, the addition of calculus content analysis, and the spatial and temporal expansion of Central Andean samples for which oral paleopathological conditions are the central data set. Multivariate statistical techniques, such as principle components analysis and General Estimating Equations, are essential for characterizing patterns and associations, and using a repeated subjects strategy can adjust for variations in the number of observations that can be made for each individual. Because oral paleopathological conditions are age-progressive, statistics that can account for variations in samples’ age-at-death profiles are essential. Creating age-based subgroups (c.f. Klau and Tam, 2009 and Williams and Murphy, 2013) for analyses often controls for demographic variation, but this process significantly decreases sample sizes, a problem that is further exacerbated when samples are also divided by other important bicultural variables such as sex, ethnic group, or geographic origin. When the resulting subsamples are examined using univariate statistical tests, there is no opportunity to consider the interaction of multiple variables, and so tracing intersectionality is not possible. As many of the above studies have shown, however, this problem can be addressed with multivariate statistical techniques. Dental calculus has not yet become a focus of Central Andean oral paleopathological studies but microscopic and biochemical analyses of dental calculus represent a new frontier that holds tremendous promise for investigating lived experience. A few analyses have made use of the presence of plant micro-fossils, but no studies of the ancient microbiome have yet been conducted. Sankaranarayanan et al. (2017), who studied the microbiomes of living Peruvian communities, comparing Amazonian foragers and central highland traditional agriculturalists to urbanized residents of two southern coastal communities, found that richness in bacterial biodiversity decreased with urbanization. It is anticipated that as researchers begin reconstructing the oral microbiome and assessing its relationship to traditional oral paleopathological conditions, skeletal health indicators, and a variety of social factors, new light will be shed on the lived experience of past Central Andean populations. The research highlighted herein demonstrates both the usefulness of oral conditions for the reconstruction of diet and habitual coca chewing, and through chronicling these activities, the possibilities for understanding shifts in economic and political systems and the integration of communities into imperial systems. Through the integration of several indicators (Table 1), the studies discussed suggest that the introduction of agricultural foods may have occurred earlier than expected, during the Archaic period, but that Central Andean populations may have maintained a mixed dietary resource strategy longer than thought, only intensifying agricultural production in the middle EIP (Table 3). Using frequencies of oral paleopathological conditions, researchers have also identified that changes accompanying Inca imperialism were likely not as detrimental to native populations as was Spanish colonialism. Finally, researchers have shown that coca chewing, a long-practiced, culturally important activity in the Andes,

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