**5. The new research agenda on the historical relation between caries and food**

The main objective of the study of caries and other dental diseases from the anthropological point of view is to recognize long term dietary changes related to historical events, with the purpose of understanding the rise of civilization as an integrated process that articulates not only new subsistence patterns and technologies but also new forms of relationship among human beings.

Bioanthropological literature offers several comparative studies of caries among groups with known subsistence patterns and social organization that indicates that dental diseases are less frequent or do not appear in hunter-gatherers, whereas they are more frequent and variable in farmers (Table 2). However, there is not simple or universal explanation for patterns of changes in caries frequencies during human history (Tayles et al., 2000, 2009).

The relationship between caries and agriculture is based on the assumption of an increase of carbohydrate in the diet and the supposition that all these carbohydrates are cariogenic. This assumption has led many scholars to infer, solely based on the increase of caries rates, the adoption of agriculture. However, the lower caries rates observed in Asiatic rice-eating farmers contradicts this assertion (Tayles et al., 2009). On the other hand, there are ethnographic records of a great variety of groups that took advantage of diverse subsistence strategies combining foods from hunting and gathering (terrestrial and/or marine), with vegetables from gathering and farming in different proportions (Hillson, 2001). These

Caries Through Time: An Anthropological Overview 21

suffers from two interproximal lesions that affect dentin and pulp. Although they have the same caries frequency and/or index it is possible that their diets are quite different (Fig. 4). Pezo & Eggers (2010) employed several dental paleopathology markers to infer past diets in four groups with different stages of agricultural development inhabiting the Peruvian North Coast and observed a paradox overlap of the simple caries frequencies and DMI that did not correspond to technological and social changes of the different epochs. In a more detailed analysis it was observed an increase in the "speed of development" of caries and a gradual change in the caries location from occlusal to extra-occlusal caries, in accordance to the expected for more cariogenic diets associated with the adoption of new vegetal products and new processing technologies that accompanied the agricultural intensification. Sweet fruits and two maize types introduced in different epochs produced totally different caries patterns. In the later period, near to the European contact, when farming technologies reached their maximum apogee, besides carious lesions and other conditions inherent of an agricultural diet, typical culturally inflicted lesions appear: those produced by coca leaf

Fig. 4. **The problem of "simple" caries frequencies and indices in Bioanthropology.** In archaeological samples similar indices do not necessarily correspond to similar dietary

These results, lead us to conclude that the use of caries indices like DMI or the record of simple caries frequencies are insufficient in reflecting known differences in agricultural development because they do not allow one to discriminate between different degrees of cariogenicity of a diet (Fig. 5). Caries depth and location are better markers to evaluate cariogenicity in past populations. The most accurate indicators are dentine caries and extraocclusal lesions. Occlusal caries are informative, but can be eliminated by intense dental wear (pulp exposures due to dental wear must then be subtracted from the total number of

chewing and maize beer or *"chicha"* beverage.

conditions and comparable caries patterns.

groups can not be classified into those two "hermetic" categories (hunter-gatherers and farmers). During the human history many societies show different civilizatory trajectories and "wide spectrum" diets.

Despite, the "typical" frequencies for each type of diet have been used in bioanthropology to infer subsistence and social organization in groups with unknown dietary record18 (Lukacs, 1992, 1996; Turner, 1978, 1979; Ubelaker, 2000), the use of "simple" caries indices and frequencies have showed limitations. These difficulties arise because of the superposition and non-specificity of the "typical" ranges and the consequent problem of classifying populations with mixed subsistence strategies or developing stages of agricultural subsistence (Godoy,2005; Hillson, 2001; Lukacs, 1992, 1996). In addition, there is a clear association between age and caries experience that is difficult to evaluate in archaeological populations. In living peoples caries progress with the age, and the proportion of teeth affected by coronal or root caries increase with age (Luan et al., 1989; Matthesen et al., 1990). In general, caries experience can be very variable among individuals, with many or few caries per individual, a situation that can obscure the perception of caries frequencies in whole populations.

Because of the fragmentary nature of the archaeological material the loss of information regarding the number of individuals affected in the population and the number of lesions in lost teeth (*antemortem* and *postmortem*19) is inevitable. Thus, since it is likely that some teeth lost antemortem should have been lost due to carious lesions, the resultant rate can be produce an under-estimative of the real caries experience of an individual or group. On the other hand, we do not know how many teeth were lost due to caries or other conditions such as trauma and periodontal disease (Carranza, 1986; Lukacs, 2007). Besides that, it is difficult to know how many teeth were present in the lost maxillary segments. For those reasons, modern caries indices such as DMFT or DMFS are unsuitable for bioarchaeological research. Also, diagenetic changes and variable preservation of skeletal series can obscure genuine differences or similarities between sites, making problematic any inter-observer comparisons (Hillson, 2001; Wesolowski, 2006).

The caries rates regularly used in bioanthropology (Duyar & Erdal, 2003; Hillson, 2001; Moore y Corbett, 1971; Lukacs, 1992, 2007; Powell, 1985; Saunders et al., 1997; Watt et al., 1997;) for being numeric, basically count the number of lesions creating a false perception that high frequencies, prevalences or caries indices, correspond to an increase of agricultural development. Furthermore, these rates do not discriminate between the type, severity or exact location of the lesions, which can be much more informative about a diet's cariogenicity. Individuals with carious lesions of different depth and location can have similar caries rates. This fact can obscure the interpretation of caries experience among populations. For instance, a young adult from a group A with two occlusal lesions that affects only enamel has the same numeric index as another young adult from a group B that

<sup>18</sup> Evaluating populations with known diets, Turner (1979) defined ranges of characteristics frequencies for each type of subsistence: 0%-5.3% for hunter-gatherers, 0.44% - 10.3% for mixed economies, and 2.2% - 26.9% for farmers.

<sup>19</sup> Approximately 15% of teeth are lost during the process of human remains recovery. These sockets are difficult to be considered for caries indexes because lost teeth could, or could not, have been affected by caries (Larsen, 1997; Pezo, 2010; Saunders et al., 1997).

groups can not be classified into those two "hermetic" categories (hunter-gatherers and farmers). During the human history many societies show different civilizatory trajectories

Despite, the "typical" frequencies for each type of diet have been used in bioanthropology to infer subsistence and social organization in groups with unknown dietary record18 (Lukacs, 1992, 1996; Turner, 1978, 1979; Ubelaker, 2000), the use of "simple" caries indices and frequencies have showed limitations. These difficulties arise because of the superposition and non-specificity of the "typical" ranges and the consequent problem of classifying populations with mixed subsistence strategies or developing stages of agricultural subsistence (Godoy,2005; Hillson, 2001; Lukacs, 1992, 1996). In addition, there is a clear association between age and caries experience that is difficult to evaluate in archaeological populations. In living peoples caries progress with the age, and the proportion of teeth affected by coronal or root caries increase with age (Luan et al., 1989; Matthesen et al., 1990). In general, caries experience can be very variable among individuals, with many or few caries per individual, a situation that can obscure the perception of caries frequencies in

Because of the fragmentary nature of the archaeological material the loss of information regarding the number of individuals affected in the population and the number of lesions in lost teeth (*antemortem* and *postmortem*19) is inevitable. Thus, since it is likely that some teeth lost antemortem should have been lost due to carious lesions, the resultant rate can be produce an under-estimative of the real caries experience of an individual or group. On the other hand, we do not know how many teeth were lost due to caries or other conditions such as trauma and periodontal disease (Carranza, 1986; Lukacs, 2007). Besides that, it is difficult to know how many teeth were present in the lost maxillary segments. For those reasons, modern caries indices such as DMFT or DMFS are unsuitable for bioarchaeological research. Also, diagenetic changes and variable preservation of skeletal series can obscure genuine differences or similarities between sites, making problematic any inter-observer

The caries rates regularly used in bioanthropology (Duyar & Erdal, 2003; Hillson, 2001; Moore y Corbett, 1971; Lukacs, 1992, 2007; Powell, 1985; Saunders et al., 1997; Watt et al., 1997;) for being numeric, basically count the number of lesions creating a false perception that high frequencies, prevalences or caries indices, correspond to an increase of agricultural development. Furthermore, these rates do not discriminate between the type, severity or exact location of the lesions, which can be much more informative about a diet's cariogenicity. Individuals with carious lesions of different depth and location can have similar caries rates. This fact can obscure the interpretation of caries experience among populations. For instance, a young adult from a group A with two occlusal lesions that affects only enamel has the same numeric index as another young adult from a group B that

18 Evaluating populations with known diets, Turner (1979) defined ranges of characteristics frequencies for each type of subsistence: 0%-5.3% for hunter-gatherers, 0.44% - 10.3% for mixed economies, and

19 Approximately 15% of teeth are lost during the process of human remains recovery. These sockets are difficult to be considered for caries indexes because lost teeth could, or could not, have been affected by

and "wide spectrum" diets.

whole populations.

2.2% - 26.9% for farmers.

comparisons (Hillson, 2001; Wesolowski, 2006).

caries (Larsen, 1997; Pezo, 2010; Saunders et al., 1997).

suffers from two interproximal lesions that affect dentin and pulp. Although they have the same caries frequency and/or index it is possible that their diets are quite different (Fig. 4).

 Pezo & Eggers (2010) employed several dental paleopathology markers to infer past diets in four groups with different stages of agricultural development inhabiting the Peruvian North Coast and observed a paradox overlap of the simple caries frequencies and DMI that did not correspond to technological and social changes of the different epochs. In a more detailed analysis it was observed an increase in the "speed of development" of caries and a gradual change in the caries location from occlusal to extra-occlusal caries, in accordance to the expected for more cariogenic diets associated with the adoption of new vegetal products and new processing technologies that accompanied the agricultural intensification. Sweet fruits and two maize types introduced in different epochs produced totally different caries patterns. In the later period, near to the European contact, when farming technologies reached their maximum apogee, besides carious lesions and other conditions inherent of an agricultural diet, typical culturally inflicted lesions appear: those produced by coca leaf chewing and maize beer or *"chicha"* beverage.

Fig. 4. **The problem of "simple" caries frequencies and indices in Bioanthropology.** In archaeological samples similar indices do not necessarily correspond to similar dietary conditions and comparable caries patterns.

These results, lead us to conclude that the use of caries indices like DMI or the record of simple caries frequencies are insufficient in reflecting known differences in agricultural development because they do not allow one to discriminate between different degrees of cariogenicity of a diet (Fig. 5). Caries depth and location are better markers to evaluate cariogenicity in past populations. The most accurate indicators are dentine caries and extraocclusal lesions. Occlusal caries are informative, but can be eliminated by intense dental wear (pulp exposures due to dental wear must then be subtracted from the total number of

Caries Through Time: An Anthropological Overview 23

**(%)** 

**Subsistence pattern** 

Huntergatherers

Fishermen

Fisher-

Farmers

**Population Frequency** 

**Hunter-gatherers (Turner, 1979) 0 – 5.3** 

Oklahoma-USA, Fourche Maline, Archaic (Powell, 1985) 0.07 Cis-Baikal-Siberia, Neolithic Kitoy (Lieverse et al., 2007) 0.23 Patagonia, NW-MZ Final Late Holocene (Bernal et al., 2007) 3.30 Patagonia, NW-MZ Early Late Holocene (Bernal et al., 2007) 5.19 Central Brazil, Paleoindian (Neves & Cornero, 1997) 9.00 Portugal, Mesolithic (Lubell et al., 1994) 14.30 **Mixed diet (Turner, 1979) 0.4 – 10.3** 

Alaska, Esquimos pre-contact (Keenleyside, 1998) <0.05

2005) 0.40 Northern Chile (3500–2000 BC) (Kelley et al., 1991) 0.60 Patagonia, NE-RN Middle Late Holocene (Bernal et al., 2007) 0.95 Alaska, Ipiutak pre-contact (Costa, 1980) 14.40 Gran Canaria, coastal mounds (Delgado et al., 2006) 6.20

Peruvian Coast, Early Formative (Pezo & Eggers, 2010) 21.60 **Farmers (Turner, 1979) 2.2 – 26.9** 

Portugal, Neolithic (Lubell et al., 1994) 3.10 China, Ying Shang period (Sakashita et al., 1997) 3.45 Pakistan, Harappa-Bronze Age (Lukacs, 1992) 6.80 Turkey, Bizantines 13 th century (Caglar et al., 2007) 6.80 Florida-USA, Early Mission 1600-1680 (Larsen et al., 2007) 7.40 Georgia-USA, Early Mission 1600-1680 (Larsen et al., 2007) 7.60 England, Roman 43-410 AD (Roberts & Cox, 2007) 7.50 Patagonia, CW-SJFLH Late Holocene (Bernal et al., 2007) 10.17 Sweden, 17 th century (Lingström & Borrman, 1999) 12.00 Northern Chile, Maitas (Kelley et al., 1991) 14.40 Gran Canaria-inland caves (Delgado et al., 2006) 15.70 Oman, Iron Age (Nelson & Lukacs, 1994) 18.00 Peruvian Coast, Middle Formative (Pezo & Eggers, 2010) 21.73 Peruvian Coast, Epiformative (Pezo & Eggers, 2010) 20.67 Peruvian Coast, Late Intermediate Period (Pezo & Eggers, 2010) 22.07 Florida-USA, Late Mission 1680-1700 (Larsen et al., 2007) 24.40 Texas-USA, Confederate Veterans (Denseizer & Baker, 2004) 24.40 High Canada, 19th century (Saunders et al., 1997) 35.95 Northern Chile, Quitor-5 (Kelley et al., 1991) 48.10

Table 2. Caries frequencies and subsistence patterns among past populations

gardeners Early Hawaians (Keene, 1986) 9.80

Brazilian Shellmound, Middle Holocene (Okumura & Eggers,

carious lesions). Other comparisons along the time have confirmed an increase of the depth of lesions and more affected dental surfaces, related to the introduction of more cariogenic foods (Bonfiglioli et al., 2003; Hillson, 2001, Godoy, 2005; Pechenkina et al., 2002; Sakashita et al., 1997).

Then, the new challenge of oral paleopathology is to determine the impact of farming of different kinds of crops in different parts of the world by the observation of caries depth and location patterns associated with different diets. Rather than a particular indicator, the "ideal method" for paleodietary reconstruction with oral pathology is the characterization of specific "paleopathological models" produced by the integration of caries, periodontal disease and dental wear patterns obtained through the maximum possible number of markers. Caries depth and location as well as other oral conditions need to be considered in the context of oral ecology. Only an integrative analysis, relying also on as much archaeological data20 (concerning the contextual social conditions) and bioanthropological evidence as possible can result in more reliable reconstructions of ancient diet.

Fig. 5. **Pathological profiles in archaeological samples from the Central Andean Coast.** a) Fisherman with incipient agriculture (around 2400 BC). b) Fully developed farmer with coca leaf chewing habit (around 1300 AD).

<sup>20</sup> The methods commonly used for paleodietary reconstruction are: a) the identification of botanical and zoological macro-remains from excavations; b) the physico-chemical analyses (stable isotopes and traces) in bones; c) the identification of botanical micro-remains (phytoliths and starch granules) from dental calculus, coprolites and artifacts (Fry, 2006; Pearsall, 2000).

carious lesions). Other comparisons along the time have confirmed an increase of the depth of lesions and more affected dental surfaces, related to the introduction of more cariogenic foods (Bonfiglioli et al., 2003; Hillson, 2001, Godoy, 2005; Pechenkina et al., 2002; Sakashita

Then, the new challenge of oral paleopathology is to determine the impact of farming of different kinds of crops in different parts of the world by the observation of caries depth and location patterns associated with different diets. Rather than a particular indicator, the "ideal method" for paleodietary reconstruction with oral pathology is the characterization of specific "paleopathological models" produced by the integration of caries, periodontal disease and dental wear patterns obtained through the maximum possible number of markers. Caries depth and location as well as other oral conditions need to be considered in the context of oral ecology. Only an integrative analysis, relying also on as much archaeological data20 (concerning the contextual social conditions) and bioanthropological

evidence as possible can result in more reliable reconstructions of ancient diet.

Fig. 5. **Pathological profiles in archaeological samples from the Central Andean Coast.** a) Fisherman with incipient agriculture (around 2400 BC). b) Fully developed farmer with coca

20 The methods commonly used for paleodietary reconstruction are: a) the identification of botanical and zoological macro-remains from excavations; b) the physico-chemical analyses (stable isotopes and traces) in bones; c) the identification of botanical micro-remains (phytoliths and starch granules) from

leaf chewing habit (around 1300 AD).

dental calculus, coprolites and artifacts (Fry, 2006; Pearsall, 2000).

et al., 1997).


Table 2. Caries frequencies and subsistence patterns among past populations

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#### **6. Acknowledgments**

The authors wish to thank Adriana Andrade for the text revision, Maria Mestriner and Suely Praty from the *Biblioteca da Faculdade de Odontologia da Universidade de São Paulo (USP)*, Walter Neves from Laboratório de Estudos Evolutivos Humanos IBUSP, and the support of FAPESP: 2011/503399 and CNPq-bolsa de produtividade.

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**2** 

**Socioeconomic Influence on Caries** 

**Centuries A.D., Czech Republic)** 

*2Department of Anthropology, National Museum, Prague,* 

Petra Stránská3 and Jaroslav Bruzek1,4

*Université Bordeaux1, Talence,* 

*1France* 

*2,3,4Czech Republic* 

**Susceptibility in Juvenile Individuals with** 

Virginie Gonzalez-Garcin1, Gaëlle Soulard1, Petr Velemínský2,

*1UMR 5199 PACEA, Anthropologie des Populations Passées et Présentes,* 

*3Institute of Archaeology, Academy of Sciences of the Czech Republic, Prague,* 

*4Department of Anthropology, Faculty of Humanities, West Bohemian University, Pilsen,* 

Dental growth is recognized to be less influenced by environmental factors than by genetics (Halcrow & Tayles, 2008; Saunders et al., 2000; Scheuer & Black, 2000a). However, it has been demonstrated that dental health is partly conditioned by the differential enamel susceptibility of environmental attack (sugars, bacterial flora, etc.) (Hillson, 1979; Johansson et al., 1994; König & Navia, 1995; Navia, 1994). In an earlier article published in HOMO, 2010, vol. 61, p. 421-439, our results showed that there is some influence of lifestyle on dental health of juvenile individuals (Garcin et al., 2010). Four populations belonged from rural and urban, coastal and inland lifestyles were compared in that paper. We would like, in this chapter, to refine these results with the evaluation of the influence of socioeconomic status on dental health in juvenile individuals with limited dental care. The point of view is

focused on tooth development and enamel quality rather than strict caries analyses.

The influence of socioeconomic status on health is a very common topic on living populations (e.g. Alvarez & Navia, 1989; Greksa et al., 2007; Klein and Palmer, 1941; O'Sullivan et al., 1992; Van de Poel et al., 2007). One of the main biases to study these populations is the difficulty to define the environmental framework of the analysis. It is nearly the same in past populations but they have the advantage of the sample size (especially on children). However, most studies on past and historic populations evaluating both dental enamel hypoplasia and caries, are based on adult remains only (Barthelemy et al., 1999; Belcastro et al., 2007; Cucina et al., 2006; Esclassan et al., 2009; Palubeckaité et al.,

**1. Introduction** 

**Limited Dental Care: Example from an Early** 

**Middle Age Population (Great Moravia, 9th-10th**

