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 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 postmortem19) 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

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 2.2% - 26.9% for farmers.

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 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.

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 extra-occlusal 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 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).

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).

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

Population

Frequency Subsistence (%) pattern

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) Patagonia, NW-MZ Final Late Holocene (Bernal et al., 2007)

0.23 3.30

Hunter-gatherers

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

Brazilian Shellmound, Middle Holocene (Okumura & Eggers,

0.40

2005)

Fishermen

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) Early Hawaians (Keene, 1986)

6.20 9.80

Fisher-gardeners

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

Farmers

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

Table 2. Caries frequencies and subsistence patterns among past populations

Comparing peoples living in the same place at different times or groups living in different sites at the same time is more useful and informative than studying an isolated site or population. Statistical analyses, although necessary for the depuration of more important information, must not disregard qualitative analyses. A permanently pending agenda is the refinement of methods and the increase of epidemiological studies in traditional non-Occidentalized groups that can be useful for a better contextualization of future bioarchaeological studies. These research avenues would allow a much better contextualization of future bioarchaeological work. Last but not least, the better knowledge of our past diets will certainly make us better cope with the future of food production and its ecological and health consequences.

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