**4. Key factors related to caries prevalence in human populations: Physiological or cultural factors?**

Much of the studies carried out in hunter-gatherers and farmers from different latitudes and temporal periods have stated a particular trend: women show higher caries prevalences than men (Larsen et al., 1991; Lukacs, 1992, 1996, 2008, 2011; Luckacs & Largaespada, 2006; Milner, 1984; Rodríguez, 2003; Walker & Hewlett, 1990). This phenomenon suggests two possible, not necessarily excluding, explanations: a) there is a major constitutional predisposition in females to caries; b) the differences are culturally regulated.

Clinical researches of the last decades have revealed that physiological differences between sexes have an important indirect impact on oral ecology. The saliva's chemical composition and flow are modified in various manners according to hormonal fluctuations associated with puberty, menstruation, and pregnancy. These processes lead to a much more cariogenic oral environment in females than in males. Estrogen levels are positively correlated with caries rates whereas androgens do not affect them (Lukacs & Largaespada, 2006). Experimental and clinical studies show that pregnancy reduces the buffer capacity of saliva and produces xerostomy that promotes bacterial growth, increasing the susceptibility to caries (Bergdahl, 2000; Dowd, 1999; Lukacs & Largaespada, 2006; Salvolini et al., 1998; Valdéz et al., 1993).

From an evolutionary perspective, it has been suggested that the increase of fertility that accompanied the sedentary lifestyle and the adoption of agriculture had a significant effect on the increase in caries rates worldwide (Lukacs, 2008). The classic proverb "a tooth per child" expresses the traditional idea that pregnancy results in a deterioration of oral health along with a weakening in the tooth structure and subsequent caries development and tooth loss (Lukacs, 2011; Lukacs & Largaespada, 2006). However, although there is evidence of increased periodontal inflammation in women during pregnancy, tooth loss due to pregnancy is more controversial (Larsen et al., 1991; Lukacs, 2011).

From the same point of view, the fact that much more males than females show high caries frequencies have been interpreted as a cultural mechanism of adaptation, in which young men are selectively buffered from malnutrition, through the exposition to higher amounts of cariogenic foods (Slaus et al. 1997). However, women usually show more severe nutritional stress markers, such as frequent enamel hypoplasias, less intervals between defects and more frequent tooth growth disruptions (King et al., 2005).

Among other "constitutional" reasons argued for this repetitive higher prevalence of caries in women, the earlier eruption of the female dentition (that exposes the teeth for longer time), has been also mentioned. This assertion, however, has not demonstrated strong correlation with caries prevalence (Larsen, 1997). On the other hand, if the reasons were

Caries Through Time: An Anthropological Overview 19

the castle show significantly lower caries frequencies (6.4%) than ordinary village people (12.1% - Fryer, 1984). In post-medieval Europe caries tends to affect more the opulent class than the poor class due to the regular consumption of sweet foods. Since that epoch caries has been perceived as an occupational disease among bakers and confectioners (Götze et al., 1986; Kainz & Sonnabend, 1983). Historical records of the meals served for the Spanish royalty of the 18th century included meat broths and stews from hunted and breeding animals that contained wine, sugar and cinnamon, while bread was the usual side order. The last part of each main meal was the sweet dessert that included cakes, creams, sugar coated donuts, fruit tartlets, cookies, jelly, fruits with syrup, dates, pomegranates, nuts, hazelnuts, and figs. The Spanish royalty usually consumed chocolate that was the unique

From these information we can infer that, although it is true that high caries frequencies are associated to poverty and a restrict diet (rich in carbohydrates and poor in animal protein), it is also true that in some periods better economic conditions facilitated a more frequent intake of food, increasing also the amount of cariogenic substratum for certain sub-groups of the population. Other socio-economical factors must be carefully considered; among them, the unfavorable conditions of dental structure development due to malnutrition and hypocalcification that turns tooth much more vulnerable to caries attack (Alvarez, 1988; Campodónico et al., 2001; Heredia & Alva, 2005; Hollister & Weintraub, 1993). Finally, enamel defects, more common in emerging countries due to nutritional stress, can facilitate the development of carious lesions under the presence of cariogenic diets (Nikiforou &

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

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

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.,

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

food permitted during the penitence days (Pérez Samper, 2003).

Fraser, 1981).

human beings.

2000, 2009).

**food** 

strictly physiological, then differences between men and women should be universal, but in general there are many clinical and archaeological examples that suggest the existence of other factors involved (Powell, 1988; White, 1994). So, despite the plausible possibility that women show a higher intrinsic physiologic susceptibility towards caries than man, the caries experience is behaviorally mediated.

It has been observed that in populations where caries are higher in women, there is usually a differentiated consumption of foods: men consuming more meat and women consuming more carbohydrates. Contemporary foragers populations show that men, responsible for getting the protein, consumes more amounts from the meat that they hunted, whereas women, responsible for vegetables gathering, and food preparation, consume more carbohydrates during their activities (Walker & Erlandson, 1986; Walker & Hewlett, 1990). Furthermore, men eat some few "big" meals along the journey, whereas women eat several "little" ones, causing more exposition to caries (Gustafsson et al., 1953; Rugg-Gunn & Edgar, 1984; Wrangham, 2009).

Interestingly, the differences between men and women are much more subtle among farmers. However, these slight differences also seem to be related more to cultural than constitutional factors. The Bantu show high caries prevalence in accordance to their considerable intake of carbohydrates and men have higher frequencies than women (9.1% versus 7.1% - Walker & Hewlett, 1990). The same happens in some populations from South American Andes where the carious lesions (mainly cervical ones) are much more frequent in males that preserve the ancestral habit of coca leaf chewing (Pando, 1988). This pattern has also been observed in archaeological samples (Indriati & Buikstra, 2001; Langsjöen, 1996; Pezo & Eggers, 2010; Valdivia, 1980). In Andean and Amazonian populations, it was observed higher prevalence in women who are responsible for chewing maize and manioc as a part of preparing fermentable beverages (*chicha, masato, kiki* - Larsen, 1997; Pezo & Eggers, 2010).

On the other hand, we must consider the effect of social differences in the patterns of food consumption in stratified societies (Cucina & Tiesler, 2003; Gagnon, 2004; Sakashita et al., 1997). There is growing evidence suggesting that members from different social classes, consuming different foods, tend to have different patterns of dental disease. In Copán (Honduras) and Lamanai (Belize), during the Classic Maya Period, elites show lower prevalence of caries than ordinary people. Among low-status burials, there are significantly more caries than in high-status individuals. It was also observed, through an isotopic study, that low-status individuals eat mainly carbohydrates (maize). Stable isotopes studies confirmed that low-status individuals eat mainly carbohydrates (maize), whereas elite individuals consumed much less maize and had easy access to animal protein, and in general, a much varied and cariostatic diet (Reed, 1994). Contrarily, among citizens and slaves from Yin-Shang period (Anyang, China) oral diseases were significantly higher in citizens' samples (Sakashita et al., 1997). High-status individuals from the Peruvian North Coast (Late Formative, 400-1 BC) do not show more caries than their low-status contemporary ones (Gagnon, 2004).

Comparisons between social classes show contradictory results in medieval Europe. Individuals from all social classes, buried around the Westerhuss church (Sweden), do not show differences in caries prevalence that suggest similar diets independently of social status (Swardstedt, 1966). In Zalavár (Hungary), however, high class individuals linked to

strictly physiological, then differences between men and women should be universal, but in general there are many clinical and archaeological examples that suggest the existence of other factors involved (Powell, 1988; White, 1994). So, despite the plausible possibility that women show a higher intrinsic physiologic susceptibility towards caries than man, the

It has been observed that in populations where caries are higher in women, there is usually a differentiated consumption of foods: men consuming more meat and women consuming more carbohydrates. Contemporary foragers populations show that men, responsible for getting the protein, consumes more amounts from the meat that they hunted, whereas women, responsible for vegetables gathering, and food preparation, consume more carbohydrates during their activities (Walker & Erlandson, 1986; Walker & Hewlett, 1990). Furthermore, men eat some few "big" meals along the journey, whereas women eat several "little" ones, causing more exposition to caries (Gustafsson et al., 1953; Rugg-Gunn & Edgar,

Interestingly, the differences between men and women are much more subtle among farmers. However, these slight differences also seem to be related more to cultural than constitutional factors. The Bantu show high caries prevalence in accordance to their considerable intake of carbohydrates and men have higher frequencies than women (9.1% versus 7.1% - Walker & Hewlett, 1990). The same happens in some populations from South American Andes where the carious lesions (mainly cervical ones) are much more frequent in males that preserve the ancestral habit of coca leaf chewing (Pando, 1988). This pattern has also been observed in archaeological samples (Indriati & Buikstra, 2001; Langsjöen, 1996; Pezo & Eggers, 2010; Valdivia, 1980). In Andean and Amazonian populations, it was observed higher prevalence in women who are responsible for chewing maize and manioc as a part of preparing fermentable

On the other hand, we must consider the effect of social differences in the patterns of food consumption in stratified societies (Cucina & Tiesler, 2003; Gagnon, 2004; Sakashita et al., 1997). There is growing evidence suggesting that members from different social classes, consuming different foods, tend to have different patterns of dental disease. In Copán (Honduras) and Lamanai (Belize), during the Classic Maya Period, elites show lower prevalence of caries than ordinary people. Among low-status burials, there are significantly more caries than in high-status individuals. It was also observed, through an isotopic study, that low-status individuals eat mainly carbohydrates (maize). Stable isotopes studies confirmed that low-status individuals eat mainly carbohydrates (maize), whereas elite individuals consumed much less maize and had easy access to animal protein, and in general, a much varied and cariostatic diet (Reed, 1994). Contrarily, among citizens and slaves from Yin-Shang period (Anyang, China) oral diseases were significantly higher in citizens' samples (Sakashita et al., 1997). High-status individuals from the Peruvian North Coast (Late Formative, 400-1 BC) do not show more caries than their low-status

Comparisons between social classes show contradictory results in medieval Europe. Individuals from all social classes, buried around the Westerhuss church (Sweden), do not show differences in caries prevalence that suggest similar diets independently of social status (Swardstedt, 1966). In Zalavár (Hungary), however, high class individuals linked to

beverages (*chicha, masato, kiki* - Larsen, 1997; Pezo & Eggers, 2010).

caries experience is behaviorally mediated.

1984; Wrangham, 2009).

contemporary ones (Gagnon, 2004).

the castle show significantly lower caries frequencies (6.4%) than ordinary village people (12.1% - Fryer, 1984). In post-medieval Europe caries tends to affect more the opulent class than the poor class due to the regular consumption of sweet foods. Since that epoch caries has been perceived as an occupational disease among bakers and confectioners (Götze et al., 1986; Kainz & Sonnabend, 1983). Historical records of the meals served for the Spanish royalty of the 18th century included meat broths and stews from hunted and breeding animals that contained wine, sugar and cinnamon, while bread was the usual side order. The last part of each main meal was the sweet dessert that included cakes, creams, sugar coated donuts, fruit tartlets, cookies, jelly, fruits with syrup, dates, pomegranates, nuts, hazelnuts, and figs. The Spanish royalty usually consumed chocolate that was the unique food permitted during the penitence days (Pérez Samper, 2003).

From these information we can infer that, although it is true that high caries frequencies are associated to poverty and a restrict diet (rich in carbohydrates and poor in animal protein), it is also true that in some periods better economic conditions facilitated a more frequent intake of food, increasing also the amount of cariogenic substratum for certain sub-groups of the population. Other socio-economical factors must be carefully considered; among them, the unfavorable conditions of dental structure development due to malnutrition and hypocalcification that turns tooth much more vulnerable to caries attack (Alvarez, 1988; Campodónico et al., 2001; Heredia & Alva, 2005; Hollister & Weintraub, 1993). Finally, enamel defects, more common in emerging countries due to nutritional stress, can facilitate the development of carious lesions under the presence of cariogenic diets (Nikiforou & Fraser, 1981).
