**3.2 Caries: Frequencies and profiles in the last 2000 years**

Comparative analyses between Late Antique and Early Medieval populations in Europe show a clear oral health deterioration pattern with high frequencies of caries, abscesses, antemortem tooth loss, alveolar resorption and more severe dental wear in the medieval epochs due to an impoverishment in life conditions after the down of the Western Roman Empire (Belcastro et al., 2007; Manzi et al., 1999; Slaus et al., 2011).

During the Roman Imperial Age (1st–4th centuries AD) caries affects 71.6% of the individuals and 15% of the teeth from Quadrella necropolis (Isernia, Italy). Lesions are more frequent in the posterior teeth and cervical caries are more frequent than occlusal ones. Moreover, occlusal caries decrease with age while cervical ones increase (Bonfiglioli et al., 2003). In general, caries frequencies of Late Antique populations range between 4-15%, whereas in the Early Medieval sites they range between 11.7-17.5% (Slaus et al., 2011). These noticeable differences suggest a drastic change in the dietary habits with a significant increase of carbohydrates in the Early Medieval times.

Historical records state that the typical diet of the middle and low classes in the Western Roman Empire was based on: bread (rich in impurities), porridge of cereals, some pulses, vegetables, olives, some fruits and wine, as well as goats and sheeps. Throughout the Empire diet was quiet homogeneous (Dosi & Schnell., 1990). In the medieval Europe lowclass subsistence was based essentially on cereals (the bread represents the 70% of their intake) whereas the protein consumption (meat from hunting or shepherded animals and fresh fish) was low and uncommon (Mazzi, 1981).

The medieval diet of Mediterranean peasants was composed mainly by cereals, specially bread, wheat and barley, pulses (broad beans, peas, lentils, chickpeas), and fruits such as figs, olives, plums, peaches, pine kernels, almonds and grapes (Eclassan et al., 2009). In Britain the most common products were wheat, barley, oats, rye, beans, milk, cheese, eggs, bacon and fowl and the diet of the poor classes was probably restricted to coarse black bread

<sup>9</sup> Undoubtedly, corn was one of the most valuable products in the ritual and daily life within Americas. Whereas in Mesoamerica it seems that it has been cultivated almost exclusively (monoculture), in the Andes was only one of the most important crops, consumed in several ways and used to prepare *"chicha"* (maize beer) (Antúnez de Mayolo, 1981; Bonavia, 2008).

10 Contemporary Approach to Dental Caries

In pre-contact America, the consumption of starchy seed-bearing plants like chenopodiaceous, cucurbitaceous, fabaceous, asteraceous (sunflower) has been suggested as the first stage of farming (between 8000-5000 BP) and is related to the first changes in the oral pathological profiles (Bernal et al., 2007; Pezo, 2010; Piperno, 2011). The increase of caries frequency has been attributed mainly (but not exclusively) to maize consumption9 (*Zea mays* - Larsen et al., 1991; White, 1994) and more specifically to a gradual replacement of popcorn (*indurata* variety), consumed in the earliest periods, for a softer, sweeter and thus more cariogenic, amylaceous maize (*amylacea* or *saccharata* variety) during the second millennium BC (Pezo, 2010; Rodríguez, 2003). However, it is possible that due to the enormous dietary variety derivate from a multiplicity of ecological niches, there are other potentially cariogenic products such as tubercles (wild and cultivated), as well as sweet and

Comparative analyses between Late Antique and Early Medieval populations in Europe show a clear oral health deterioration pattern with high frequencies of caries, abscesses, antemortem tooth loss, alveolar resorption and more severe dental wear in the medieval epochs due to an impoverishment in life conditions after the down of the Western Roman

During the Roman Imperial Age (1st–4th centuries AD) caries affects 71.6% of the individuals and 15% of the teeth from Quadrella necropolis (Isernia, Italy). Lesions are more frequent in the posterior teeth and cervical caries are more frequent than occlusal ones. Moreover, occlusal caries decrease with age while cervical ones increase (Bonfiglioli et al., 2003). In general, caries frequencies of Late Antique populations range between 4-15%, whereas in the Early Medieval sites they range between 11.7-17.5% (Slaus et al., 2011). These noticeable differences suggest a drastic change in the dietary habits with a significant

Historical records state that the typical diet of the middle and low classes in the Western Roman Empire was based on: bread (rich in impurities), porridge of cereals, some pulses, vegetables, olives, some fruits and wine, as well as goats and sheeps. Throughout the Empire diet was quiet homogeneous (Dosi & Schnell., 1990). In the medieval Europe lowclass subsistence was based essentially on cereals (the bread represents the 70% of their intake) whereas the protein consumption (meat from hunting or shepherded animals and

The medieval diet of Mediterranean peasants was composed mainly by cereals, specially bread, wheat and barley, pulses (broad beans, peas, lentils, chickpeas), and fruits such as figs, olives, plums, peaches, pine kernels, almonds and grapes (Eclassan et al., 2009). In Britain the most common products were wheat, barley, oats, rye, beans, milk, cheese, eggs, bacon and fowl and the diet of the poor classes was probably restricted to coarse black bread

9 Undoubtedly, corn was one of the most valuable products in the ritual and daily life within Americas. Whereas in Mesoamerica it seems that it has been cultivated almost exclusively (monoculture), in the Andes was only one of the most important crops, consumed in several ways and used to prepare

sticky fruits (Bernal et al., 2007; Neves & Cornero, 1997; Pezo, 2010).

**3.2 Caries: Frequencies and profiles in the last 2000 years** 

Empire (Belcastro et al., 2007; Manzi et al., 1999; Slaus et al., 2011).

increase of carbohydrates in the Early Medieval times.

fresh fish) was low and uncommon (Mazzi, 1981).

*"chicha"* (maize beer) (Antúnez de Mayolo, 1981; Bonavia, 2008).

(Moore & Corbett, 1973). In Scandinavia, the medieval diet was basically composed of high amounts of salted herring and dried fish, but also barley porridge, turnips, cabbages, dried sour rye bread, sour milk products, some meat, and beer (Varrela, 1991). Only in Spain there was a higher consumption of sugar cane10 and rice, introduced by the Muslims during almost eight centuries of Iberia occupation (López et al., 2010). In that epoch food was much more abrasive because the flour (milled by millstones) kept some grid that was incorporated to the bread. The cooking or storage techniques using ashes, or consumption of preparations made with unclean flour or non-dehusked grain of hulled cereals such as broomcorn (*Panicum miliaceum*) or barley (*Hordeum vulgare*) were common (Eclassan et al., 2009).

People from medieval French villages of Languedoc from the 13th-14th centuries show caries frequencies of 17.5%, with frequent occlusal and approximal caries (Eclassan et al., 2009). For medieval populations of England and Scotland from the 13th -15th centuries the caries frequency vary between 6.0-7.4% (Kerr et al., 1990; Watt et al., 1997), whereas in medieval sites in Croatia from the 11th-12th centuries the prevalence of caries is 45%, with frequencies or 9.5%, identical to the reported for later sites from the 14th-15th centuries of the same region (Slaus et al., 1997; Vodanovic et al., 2005). In general, Late Medieval populations do not present frequencies significantly higher than Early Medieval populations. It suggests that in a time span of eight centuries, no significant changes in diet occurred (Vodanovic et al., 2005).

Several studies have concluded that the most common locations of caries during the medieval epoch were occlusal and cervical approximal caries, whereas interproximal ones appear rarely (Eclassan et al., 2009; Kerr et al., 1990; Vodanovic et al., 2005; Varrela, 1991; Watt et al., 1997). Meanwhile, around the 10th-11th century, some changes in the location patterns of caries in populations in Continental and Islander Europe are evident. There is a gradual reduction in cervical-approximal caries (CEJ caries11) that was more common during the Antique Age, and an increase of occlusal, buccal, and lingual lesions, that have occurred since earlier ages. These data suggest that infantile diet became softer until the final of Middle Age (Lingström & Borrman, 1999; Moore, 1993; Moore & Corbett, 1975; Varrela, 1991; Vodanovic et al., 2005; Watt et al., 1997).

The transition from Middle to Modern Age in Europe was characterized by a remarked increase of flour for bread fabrication and consumption of sugar cane. The possibility of purchasing vegetables and grains in open markets seems to have contributed to the raise of

<sup>10</sup> The earliest evidence of domestic sugar cane (8000 BC) comes from New Guinea, Southeast Asia (Sharpe, 1998). After domestication, it spreaded rapidly to southern China, Indochina and India. Sugar cane was taken to Persia during Dario's epoch, where it was discovered by the Macedonian armies in the 4th century BC. Greeks and Romans know it as a "salt from India" and imported it only for medicinal purposes due to its high cost. The crystallized sugar was discovered in India during the Gupta dynasty, around 350 AD. Muslims discovered the sugar when they invaded Persia in 642 AD and spreaded its consumption in Western Europe after they conquered Iberia in the eighth century AD. The first reference about sugar in England, where it was considered a "fine spice", dates from the Crusades epoch in 11th century. In the 12th century, Venice built some colonies near Tyre (modern Lebanon) and began to exports sugar to Europe. Sugar was taken to America in the second trip of Columbus in 1493 (Bernstein, 2009; Parker, 2011).

<sup>11</sup> These lesions have been attributed to physiological compensatory super-eruption of roots subsequent to severe occlusal wear produced by abrasive diets (Eclassan et al., 2009). However, the possible origin related to sweet beverages must be considered (Pezo, 2010; Pezo & Eggers, 2010).

Caries Through Time: An Anthropological Overview 13

Caries increase tendency seems to have been constant during the second half of the 19th century and the first half of the 20th century, worldwide. On the other hand, preventive policies against caries did not have considerable effects until the second half of 20th century. France and England were major manufacturers of toothbrushes in 19th century, but they were considered luxury articles and regular tooth brushing was not a widespread practice

Since the 1970s a striking decline in caries experiences has been observed throughout industrialized countries (Brunelle & Carlos, 1990; Shafer et al., 1983). This seems to be related to dental treatment and the introduction of fluoride13 water and toothpaste. Also, the decline in dental caries rates was due to a range of changing social factors that seem to be linked to improvements in general health indicators (**Haugejorden, 1996;** Nikiforouk, 1985; Shaw, 1985). But in emerging countries the situation is the opposite and high caries rates are associated with malnutrition, absence of health services and poor quality of life (Alvarez,

**3.3 Diet and the "main villain" in the raise of caries throughout human history** 

The available data indicates that the modern trends on caries increases start simultaneously with permanent growth intake of sucrose during the last two centuries. The hypotheses of an increase in the susceptibility or resistance diminishment by genetic reasons or the installation of a particularly cariogenic flora have not been sufficiently corroborated (De Soet & Laine, 2008; Hassell & Harris, 1995; Shuler, 2001; van Palenstein et al., 1996) while dietary changes seem to be the most reasonable answer. In the modern western world and increasingly in other regions of the globe approximately half of consumed calories comes

Until recently, several populations living in isolated areas of the world kept their ancestral ways of life (for instance, many African tribes, Inuits, South American Indians, Melanesian, Polynesian) under conditions of perfect adaptation to their environments and diets (Donnelly et al., 1977; Mayhall, 1977; Pedersen, 1971; Schamschula et al., 1980; Walker & Hewlett, 1990). Bacteriologic analyses of their dental plaques, although not extensive, show cariogenic species, but those individuals are still developing few or no caries. Otherwise, when those populations were acculturated or simply replaced their traditional diet for an "occidental refined diet", they started to develop progressively

The case of the British colony of Tristan da Cunha, a volcanic island in the South Atlantic, described several times since 1817, is famous. Until the Second World War their diet was based on fish and potatoes (from their own production) and they were visited by a ship once or twice a year. Despite their poor hygiene, the majority of them were free of caries. When the war started many factories and military stations were built on the island deeply changing the lifestyle of the population and facilitating the importation of other foodstuff.

13 The fluoride contained in water has been recognized as a control factor of caries but high amounts of fluoride can produce recognizable enamel defects that usually involve a pattern of opacity named fluorosis (Fejerskov et al., 1994). Fluorosis has been reported in archaeological series related to

consumption of phreatic waters from wells (Pezo, 2010; Valdivia, 1980).

until after the second half of 19th century (Asbell, 1992).

1988; Campodónico et al., 2001; Heredia & Alva, 2005).

from carbohydrates and almost half of it is sucrose.

destructive caries patterns.

caries and other oral diseases during that time (Bibby, 1990; López et al., 2011). In the first half of the 17th century, Scandinavian populations, with a diet based on marine products show a caries prevalence of about 60% and frequencies of approximately 13% with increases in antemortem tooth loss among the oldest individuals. Carious lesions were most common in the occlusal area, CEJ and interproximal surfaces predominantly in lower molars. In these populations, lesions are uncommon in children but appear earlier in young adults (Lingstrom & Borrman, 1999; Mellquist & Sandberg, 1939; Varrela, 1991).

Since the 17th century, and especially during 18th century, many kinds of foods were brought from America to Europe. Among them are: maize, beans, potatoes, tomatoes, cocoa, coffee and sugar (Prats & Rey, 2003). Although sugar and sugar cane came to the West from India carried by the army of Alexander the Great in 327 BC, the "white sugar" had not became a commercial product until the 7th century. It was largely distributed until the final of 12th century(Bernstein, 2009), but it has only been imported in large scales from America to Europe since 1550 AD when sugar cane plantations increased in Brazil and in the Caribbean islands (Saunders et al., 1997; Parker, 2011). The effect of refined food on caries trends can be observed clearly in Europe during the 18th century and coincides with the increase in the production of refined sugar and the introduction of flour mills.

Populations from the 11th century cemeteries, that were excavated in Britain, Canada and USA show caries frequencies over 35% and a high number of antemortem tooth loss due to caries mostly on inferior molars. For that epoch, changes follow the same trend: cervical lesions (CEJ caries) are less common and more lesions appear in the occlusal surfaces and interproximal contact areas (Moore, 1993; Moore & Corbett, 1975; Saunders et al., 1997).

In the North American colonial diet, meat (pork, beef, and mutton), bread, and vegetables were the staples, and sweet-baked goods were also popular. Maple sugar, maize (used as corn meal flour), pumpkins, and wild fruits were harvested as well. The recipes were all almost the same, and people consumed three meals a day. The use of refined flour for the production of bread and pastries seems to have been very important and bread is still one of the most important items. In addition, the use of corn meal porridge, cooked, sweetened flour mixtures and stewed, sweetened fruits probably contributed to the cariogenicity12 of the diet (Boyce, 1972; Moore, 1993; Saunders et al., 1997).

However, those remarkable caries increments, occurred during the second half of the 19th century, have been attributed to dramatic increases in the intake of sugar and refined carbohydrates between 1830 and 1880 (Corbett & Moore, 1975; Moore, 1993). Since 1860 the importation of cane caused impressive improvements in per-capita consumption (Saunders et al., 1997). In the 1840 decade England, USA and Canada had an approximate consumption of 30 lb/person. At the end of the century those amounts raised to around 80 lb in England, 60 lb in USA and 50 lbs. in Canada (Boyce, 1972; Saunders et al., 1997). Besides, the introduction of ceramic mills in North America in 1875 (Leung, 1981), produced flours of better quality that favored its industrialization and massive consumption (Boyce, 1972).

<sup>12</sup> A cariogenic diet has been defined by the following features: frequent intake of meals with a high content of carbohydrates quickly fermentable (mainly sucrose) with retentive and sticky consistence that produces repetitive lowering of pH values and changes in the ecology of dental plaque. The cariogenic diet produces increase and quicker development of lesions, and location in non-retentive surfaces (Nikiforouk, 1985; Rugg-Gunn & Hackett, 1993).

caries and other oral diseases during that time (Bibby, 1990; López et al., 2011). In the first half of the 17th century, Scandinavian populations, with a diet based on marine products show a caries prevalence of about 60% and frequencies of approximately 13% with increases in antemortem tooth loss among the oldest individuals. Carious lesions were most common in the occlusal area, CEJ and interproximal surfaces predominantly in lower molars. In these populations, lesions are uncommon in children but appear earlier in young adults

Since the 17th century, and especially during 18th century, many kinds of foods were brought from America to Europe. Among them are: maize, beans, potatoes, tomatoes, cocoa, coffee and sugar (Prats & Rey, 2003). Although sugar and sugar cane came to the West from India carried by the army of Alexander the Great in 327 BC, the "white sugar" had not became a commercial product until the 7th century. It was largely distributed until the final of 12th century(Bernstein, 2009), but it has only been imported in large scales from America to Europe since 1550 AD when sugar cane plantations increased in Brazil and in the Caribbean islands (Saunders et al., 1997; Parker, 2011). The effect of refined food on caries trends can be observed clearly in Europe during the 18th century and coincides with the increase in the

Populations from the 11th century cemeteries, that were excavated in Britain, Canada and USA show caries frequencies over 35% and a high number of antemortem tooth loss due to caries mostly on inferior molars. For that epoch, changes follow the same trend: cervical lesions (CEJ caries) are less common and more lesions appear in the occlusal surfaces and interproximal contact areas (Moore, 1993; Moore & Corbett, 1975; Saunders et al., 1997).

In the North American colonial diet, meat (pork, beef, and mutton), bread, and vegetables were the staples, and sweet-baked goods were also popular. Maple sugar, maize (used as corn meal flour), pumpkins, and wild fruits were harvested as well. The recipes were all almost the same, and people consumed three meals a day. The use of refined flour for the production of bread and pastries seems to have been very important and bread is still one of the most important items. In addition, the use of corn meal porridge, cooked, sweetened flour mixtures and stewed, sweetened fruits probably contributed to the cariogenicity12 of

However, those remarkable caries increments, occurred during the second half of the 19th century, have been attributed to dramatic increases in the intake of sugar and refined carbohydrates between 1830 and 1880 (Corbett & Moore, 1975; Moore, 1993). Since 1860 the importation of cane caused impressive improvements in per-capita consumption (Saunders et al., 1997). In the 1840 decade England, USA and Canada had an approximate consumption of 30 lb/person. At the end of the century those amounts raised to around 80 lb in England, 60 lb in USA and 50 lbs. in Canada (Boyce, 1972; Saunders et al., 1997). Besides, the introduction of ceramic mills in North America in 1875 (Leung, 1981), produced flours of better quality that

12 A cariogenic diet has been defined by the following features: frequent intake of meals with a high content of carbohydrates quickly fermentable (mainly sucrose) with retentive and sticky consistence that produces repetitive lowering of pH values and changes in the ecology of dental plaque. The cariogenic diet produces increase and quicker development of lesions, and location in non-retentive

(Lingstrom & Borrman, 1999; Mellquist & Sandberg, 1939; Varrela, 1991).

production of refined sugar and the introduction of flour mills.

the diet (Boyce, 1972; Moore, 1993; Saunders et al., 1997).

favored its industrialization and massive consumption (Boyce, 1972).

surfaces (Nikiforouk, 1985; Rugg-Gunn & Hackett, 1993).

Caries increase tendency seems to have been constant during the second half of the 19th century and the first half of the 20th century, worldwide. On the other hand, preventive policies against caries did not have considerable effects until the second half of 20th century. France and England were major manufacturers of toothbrushes in 19th century, but they were considered luxury articles and regular tooth brushing was not a widespread practice until after the second half of 19th century (Asbell, 1992).

Since the 1970s a striking decline in caries experiences has been observed throughout industrialized countries (Brunelle & Carlos, 1990; Shafer et al., 1983). This seems to be related to dental treatment and the introduction of fluoride13 water and toothpaste. Also, the decline in dental caries rates was due to a range of changing social factors that seem to be linked to improvements in general health indicators (**Haugejorden, 1996;** Nikiforouk, 1985; Shaw, 1985). But in emerging countries the situation is the opposite and high caries rates are associated with malnutrition, absence of health services and poor quality of life (Alvarez, 1988; Campodónico et al., 2001; Heredia & Alva, 2005).

### **3.3 Diet and the "main villain" in the raise of caries throughout human history**

The available data indicates that the modern trends on caries increases start simultaneously with permanent growth intake of sucrose during the last two centuries. The hypotheses of an increase in the susceptibility or resistance diminishment by genetic reasons or the installation of a particularly cariogenic flora have not been sufficiently corroborated (De Soet & Laine, 2008; Hassell & Harris, 1995; Shuler, 2001; van Palenstein et al., 1996) while dietary changes seem to be the most reasonable answer. In the modern western world and increasingly in other regions of the globe approximately half of consumed calories comes from carbohydrates and almost half of it is sucrose.

Until recently, several populations living in isolated areas of the world kept their ancestral ways of life (for instance, many African tribes, Inuits, South American Indians, Melanesian, Polynesian) under conditions of perfect adaptation to their environments and diets (Donnelly et al., 1977; Mayhall, 1977; Pedersen, 1971; Schamschula et al., 1980; Walker & Hewlett, 1990). Bacteriologic analyses of their dental plaques, although not extensive, show cariogenic species, but those individuals are still developing few or no caries. Otherwise, when those populations were acculturated or simply replaced their traditional diet for an "occidental refined diet", they started to develop progressively destructive caries patterns.

The case of the British colony of Tristan da Cunha, a volcanic island in the South Atlantic, described several times since 1817, is famous. Until the Second World War their diet was based on fish and potatoes (from their own production) and they were visited by a ship once or twice a year. Despite their poor hygiene, the majority of them were free of caries. When the war started many factories and military stations were built on the island deeply changing the lifestyle of the population and facilitating the importation of other foodstuff.

<sup>13</sup> The fluoride contained in water has been recognized as a control factor of caries but high amounts of fluoride can produce recognizable enamel defects that usually involve a pattern of opacity named fluorosis (Fejerskov et al., 1994). Fluorosis has been reported in archaeological series related to consumption of phreatic waters from wells (Pezo, 2010; Valdivia, 1980).

Caries Through Time: An Anthropological Overview 15

were refined for cooking. In this case, by *in vitro* studies, caries increase was attributed to the absence of phytate, an organic phosphate contained in cereals that can be extracted easily by boyling (Bowen, 1994; Osborn & Noriskin, 1937). Thus, the softer texture and the

On the other hand, there are some foods that inhibit the formation of caries. Diets rich in meat lead to low caries frequencies due to the fatty acids' antibacterial power and their capacity to reduce the adherence of plaque on dental surfaces. The intake of dairy products and fish (foods rich in calcium and casein that can increase urea concentration) modifies pH values and the quantity of salivary production, inhibiting the formation of dental plaque. Finally, a food rich in polyphenols (such as cacao, coffee and tea) inhibits the bacterial metabolism and stimulates the salivary secretion representing, thus, another mechanism of

Caries frequencies of only 0.3% - 0.6%, with prevalence of around 4% have been reported for the Inuit from Angmagssalik (East Greenland), isolated until 1884 and with a diet based on meat and fish, almost without carbohydrates. These observations are in accordance with prevalences of 0.4% - 2.5% and frequencies of 0.08% - 0.35% (mainly little carious lesions in molar fissures) in craniums of ancient Inuits and are strikingly different from that observed in neighboring populations with access to sugar and cereals (Mayhall, 1977; Pedersen 1947, 1952). Little changes in the type of carbohydrate, texture, mode of conservation and preparing of meals can produce utterly different caries experiences (Molnar, 1972; Rodríguez, 2003; Turner, 1979). In Paleolithic and Mesolithic populations it is common to observe the effects of an abrasive and non-refined diet. The ancient people show an aggressive dental wear that frequently surpasses the speed of development of little aggressive carious lesion, producing an exposure of the pulp chamber with abscesses formation and consequent tooth loss (Fig. 3). In Neolithic populations the change to better processed diets gradually leads to a low wear of masticatory surfaces that is another factor why the occlusal caries could have developed earlier. This competitive relation between dental wear16 and caries has been also observed in fishermen from the South American Pacific coast, Dutch sailors from 18th -19th centuries and in other populations with marine subsistence (Milner, 1984; Maat & Van der Velde, 1987; Pezo & Eggers, 2010). Finally, dental wear is a factor that can distort the real

elimination of "protective factors" through cooking increase cariogenicity.

caries prevention (Bowen, 1994; Touger-Decker & Loveren, 2003).

perception of caries experience in several populations with abrasive diet.

However, there are also some cases that have reported a positive correlation between caries and dental wear, as observed in Mesolithic populations from Portugal and Sicily (Meiklejhon et al., 1988; Lubell et al., 1994) where the consumption of honey, figs and sweet fruits accelerates the installation of caries in attrition surfaces. This phenomenon has also been noticed for the Pecos from South West -USA during the Archaic Period (4000-1000 BC) with caries prevalence of 14% and pulp chamber exposure as the main cause of tooth loss (Larsen, 1997). Thus, the cariogenic capacity of natural sugars contained in honey and sweet

16 Dental wear is related to the physical consistence of food, the storage ways and the technology used in their processing. Analyses of coprolites (fossilized faeces) have shown some abrasive material such as phytolithes (microscopic silica structures contained in certain plant organs), seeds, little bone fragments and oxalate calcium crystals from some species (Larsen, 1997; Pearsall, 2000). Besides, historical and ethnographical data from several regions of the world describe the ingestion of abrasives such as ashes and clays as part of the meals (Antúnez de Mayolo, 1981; Indriati & Buikstra, 2001; Rodríguez, 2003).

The deterioration of their oral conditions was evident in the beginning of the 1950's. In 1962, when the volcanic activity obliged inhabitants to evacuate towards England, more than 40 % of their teeth were affected by caries or had been destroyed. The most notable change in life conditions of those individuals was diet, with a decrease in the consumption of potatoes and a compensatory consumption of sugar. It is estimated that the daily consumption of sugar rose from 1.8 g. in 1938 to 150 g. in 1966, three years after their return from England. On the other hand, under equivalent conditions, older people did not seem to be as resistant as their descendents (Holloway et al., 1963). Data that confirms this tendency have also been reported for populations from developing countries (Corraini et al., 2009; Ismail et al., 1997; Petersen & Kaka, 1999; Petersen & Razanamihaja, 1996).

Whereas the role of sugar as the main "villain" in the caries etiology seems to be evident, it is disputable if starches play a similar role (Tayles et al., 2000, 2009). By their slow accumulation in dental plaque and slower oral digestion, starch could have a relative low cariogenicity and its importance as a factor of caries depends on the simultaneous intake with sucrose as well as the frequency of its consumption (Frostell et al., 1967). Thus, starch has been defined as "co-cariogenic", especially when it is gelatinized by thermal effect (Grenby, 1997). The gelatinization of starch14 seems to be the determining factor of its cariogenicity, because in general, only gelatinized starches are susceptible to enzymatic breakage (through salivary or bacterial pocesses) to produce highly cariogenic molecules (Grenby, 1997; Lingström et al., 2000). Nevertheless, the necessary temperature for starch gelatinization surpasses 80ºC in most of the cases.

In this sense, the invention of pottery (the earliest pottery appeared in the Samara region of South-Eastern Russia about 7000 BC – Anthony, 2007), its spread and common use for storage and cooking could have been a significant trigger for the raise of caries markers before the popularization of refined sucrose consumption. Until the introduction of pottery, other cooking methods were employed around the world, but those methods would hardly result in gelatinization of starche15 (Antúnez de Mayolo, 1981; Pezo, 2010; Wrangham, 2009). The refinement and cooking of carbohydrates produce an increase in their retentive and sticky capacity the tooth surface leading to slower clearance times. For instance, bread starch shows higher clearance times than starches from potatoes or rice (Grenby, 1997; Lingström et al., 2000).

According to some authors, cooking can eliminate some protective agents (against the caries) of certain foodstuff. The Bantu of Africa show an increase in caries frequency after the adoption of a colonial diet. The amount of cereals and sugar were the same, but they

<sup>14</sup> During the process of cooking food, the starch granules are disintegrated by heat and mechanical forces. Eventually the liberation of the molecules in a process named gelatinization occurs. The temperature and water-starch proportion necessary to gelatinization are very variable in accordance to each distinct starches. For instance, the temperature for rice gelatinization ranges between 85-111°C with a proportion water-starch of 2.0-0.75 and ranges between 65-90ºC for maize starch (Lingström et al., 2000; Donald, 2004).

<sup>15</sup> These traditional methods include: a) the use of heated stones for boiling liquids within pumpkins and squashes; they were also used to roast meat and vegetables by direct contact or placed along with the food into the underground ovens covered with earth; b) roasting by direct contact with fire (as for mollusks or turtles); c) roasting of meat and vegetables wrapped in leaves or packed in bamboo canes over wood grills, among others.

14 Contemporary Approach to Dental Caries

The deterioration of their oral conditions was evident in the beginning of the 1950's. In 1962, when the volcanic activity obliged inhabitants to evacuate towards England, more than 40 % of their teeth were affected by caries or had been destroyed. The most notable change in life conditions of those individuals was diet, with a decrease in the consumption of potatoes and a compensatory consumption of sugar. It is estimated that the daily consumption of sugar rose from 1.8 g. in 1938 to 150 g. in 1966, three years after their return from England. On the other hand, under equivalent conditions, older people did not seem to be as resistant as their descendents (Holloway et al., 1963). Data that confirms this tendency have also been reported for populations from developing countries (Corraini et al., 2009;

Whereas the role of sugar as the main "villain" in the caries etiology seems to be evident, it is disputable if starches play a similar role (Tayles et al., 2000, 2009). By their slow accumulation in dental plaque and slower oral digestion, starch could have a relative low cariogenicity and its importance as a factor of caries depends on the simultaneous intake with sucrose as well as the frequency of its consumption (Frostell et al., 1967). Thus, starch has been defined as "co-cariogenic", especially when it is gelatinized by thermal effect (Grenby, 1997). The gelatinization of starch14 seems to be the determining factor of its cariogenicity, because in general, only gelatinized starches are susceptible to enzymatic breakage (through salivary or bacterial pocesses) to produce highly cariogenic molecules (Grenby, 1997; Lingström et al., 2000). Nevertheless, the necessary temperature for starch

In this sense, the invention of pottery (the earliest pottery appeared in the Samara region of South-Eastern Russia about 7000 BC – Anthony, 2007), its spread and common use for storage and cooking could have been a significant trigger for the raise of caries markers before the popularization of refined sucrose consumption. Until the introduction of pottery, other cooking methods were employed around the world, but those methods would hardly result in gelatinization of starche15 (Antúnez de Mayolo, 1981; Pezo, 2010; Wrangham, 2009). The refinement and cooking of carbohydrates produce an increase in their retentive and sticky capacity the tooth surface leading to slower clearance times. For instance, bread starch shows higher clearance times than starches from potatoes or rice (Grenby, 1997; Lingström

According to some authors, cooking can eliminate some protective agents (against the caries) of certain foodstuff. The Bantu of Africa show an increase in caries frequency after the adoption of a colonial diet. The amount of cereals and sugar were the same, but they

14 During the process of cooking food, the starch granules are disintegrated by heat and mechanical forces. Eventually the liberation of the molecules in a process named gelatinization occurs. The temperature and water-starch proportion necessary to gelatinization are very variable in accordance to each distinct starches. For instance, the temperature for rice gelatinization ranges between 85-111°C with a proportion water-starch of 2.0-0.75 and ranges between 65-90ºC for maize starch (Lingström et

15 These traditional methods include: a) the use of heated stones for boiling liquids within pumpkins and squashes; they were also used to roast meat and vegetables by direct contact or placed along with the food into the underground ovens covered with earth; b) roasting by direct contact with fire (as for mollusks or turtles); c) roasting of meat and vegetables wrapped in leaves or packed in bamboo canes

Ismail et al., 1997; Petersen & Kaka, 1999; Petersen & Razanamihaja, 1996).

gelatinization surpasses 80ºC in most of the cases.

et al., 2000).

al., 2000; Donald, 2004).

over wood grills, among others.

were refined for cooking. In this case, by *in vitro* studies, caries increase was attributed to the absence of phytate, an organic phosphate contained in cereals that can be extracted easily by boyling (Bowen, 1994; Osborn & Noriskin, 1937). Thus, the softer texture and the elimination of "protective factors" through cooking increase cariogenicity.

On the other hand, there are some foods that inhibit the formation of caries. Diets rich in meat lead to low caries frequencies due to the fatty acids' antibacterial power and their capacity to reduce the adherence of plaque on dental surfaces. The intake of dairy products and fish (foods rich in calcium and casein that can increase urea concentration) modifies pH values and the quantity of salivary production, inhibiting the formation of dental plaque. Finally, a food rich in polyphenols (such as cacao, coffee and tea) inhibits the bacterial metabolism and stimulates the salivary secretion representing, thus, another mechanism of caries prevention (Bowen, 1994; Touger-Decker & Loveren, 2003).

Caries frequencies of only 0.3% - 0.6%, with prevalence of around 4% have been reported for the Inuit from Angmagssalik (East Greenland), isolated until 1884 and with a diet based on meat and fish, almost without carbohydrates. These observations are in accordance with prevalences of 0.4% - 2.5% and frequencies of 0.08% - 0.35% (mainly little carious lesions in molar fissures) in craniums of ancient Inuits and are strikingly different from that observed in neighboring populations with access to sugar and cereals (Mayhall, 1977; Pedersen 1947, 1952).

Little changes in the type of carbohydrate, texture, mode of conservation and preparing of meals can produce utterly different caries experiences (Molnar, 1972; Rodríguez, 2003; Turner, 1979). In Paleolithic and Mesolithic populations it is common to observe the effects of an abrasive and non-refined diet. The ancient people show an aggressive dental wear that frequently surpasses the speed of development of little aggressive carious lesion, producing an exposure of the pulp chamber with abscesses formation and consequent tooth loss (Fig. 3). In Neolithic populations the change to better processed diets gradually leads to a low wear of masticatory surfaces that is another factor why the occlusal caries could have developed earlier. This competitive relation between dental wear16 and caries has been also observed in fishermen from the South American Pacific coast, Dutch sailors from 18th -19th centuries and in other populations with marine subsistence (Milner, 1984; Maat & Van der Velde, 1987; Pezo & Eggers, 2010). Finally, dental wear is a factor that can distort the real perception of caries experience in several populations with abrasive diet.

However, there are also some cases that have reported a positive correlation between caries and dental wear, as observed in Mesolithic populations from Portugal and Sicily (Meiklejhon et al., 1988; Lubell et al., 1994) where the consumption of honey, figs and sweet fruits accelerates the installation of caries in attrition surfaces. This phenomenon has also been noticed for the Pecos from South West -USA during the Archaic Period (4000-1000 BC) with caries prevalence of 14% and pulp chamber exposure as the main cause of tooth loss (Larsen, 1997). Thus, the cariogenic capacity of natural sugars contained in honey and sweet

<sup>16</sup> Dental wear is related to the physical consistence of food, the storage ways and the technology used in their processing. Analyses of coprolites (fossilized faeces) have shown some abrasive material such as phytolithes (microscopic silica structures contained in certain plant organs), seeds, little bone fragments and oxalate calcium crystals from some species (Larsen, 1997; Pearsall, 2000). Besides, historical and ethnographical data from several regions of the world describe the ingestion of abrasives such as ashes and clays as part of the meals (Antúnez de Mayolo, 1981; Indriati & Buikstra, 2001; Rodríguez, 2003).

Caries Through Time: An Anthropological Overview 17

As we can see, the historical evaluation of caries allows us to recognize some trends and recurrences in prevalences, frequencies and patterns. Although in general it is possible to identify some critical variables such as the excessive consumption of refined sucrose or gelatinized starches as etiological agents, there are many other socio-historical factors, specific for each population, that must be considered before generalizing about the complex

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

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;

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

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

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

**4. Key factors related to caries prevalence in human populations:** 

predisposition in females to caries; b) the differences are culturally regulated.

pregnancy is more controversial (Larsen et al., 1991; Lukacs, 2011).

more frequent tooth growth disruptions (King et al., 2005).

relationship between caries and subsistence pattern.

**Physiological or cultural factors?** 

Valdéz et al., 1993).

fruits such as carob, figs, and prickly pear might not be understated because they have been noticed as responsible for the high caries prevalence in some populations (Bernal et al., 2007; Nelson et al., 1999; Neves & Cornero, 1997; Pezo, 2010).

Fig. 3. **Competitive relation between caries and dental wear in an individual with abrasive diet.** Carious lesions almost eliminated through dental wear in molars, and pulp chamber exposure due to severe wear in anterior teeth.

Finally, drastic climatic changes, complex social processes, and wars can lead to resource searching by strategies considered "regressive", as well as technological innovations (Hillson, 2001; Molnar, 1972). Walker & Erlandson (1986) studied caries and dietary changes in Santa Rosa Island (Santa Barbara Channel, South California), during a time span from 4000 to 400 BP, observing that in the first 1500 years predominantly terrestrial products such as starchy roots and tubers were exploited, and later they readapted their subsistence strategies to marine sources dropped from 13.3 to 6.3% in the caries frequencies, following the reduction in carbohydrates intake.

On the other hand, there are some exceptions about the correspondence between agriculture and caries. Several groups of modern farmers with a diet based almost exclusively on starch rich foods such as taro, sweet potato, and manioc, show low caries frequencies (Barmes et al., 1970; Baume 1969). In populations from Eastern Asia, the consumption of rice, despite their frequency, has produced low caries experiences (Tayles et al., 2000). Other especially high values of caries in populations with hunter-gatherers technology have been attributed to the consumption of cariogenic species traded with neighbor farmers17 (Lukacs, 1990; Walker & Hewlett, 1990).

<sup>17</sup> African pigmies (Aka, Mbuti, Efe) traded meat and honey with the Bantu, who provided back manioc, maize, nuts, rice and plantains. In these hunter-gatherers honey is an important dietary source during great part of the year (Walker & Hewlett, 1990).

fruits such as carob, figs, and prickly pear might not be understated because they have been noticed as responsible for the high caries prevalence in some populations (Bernal et al., 2007;

Fig. 3. **Competitive relation between caries and dental wear in an individual with abrasive diet.** Carious lesions almost eliminated through dental wear in molars, and pulp

Finally, drastic climatic changes, complex social processes, and wars can lead to resource searching by strategies considered "regressive", as well as technological innovations (Hillson, 2001; Molnar, 1972). Walker & Erlandson (1986) studied caries and dietary changes in Santa Rosa Island (Santa Barbara Channel, South California), during a time span from 4000 to 400 BP, observing that in the first 1500 years predominantly terrestrial products such as starchy roots and tubers were exploited, and later they readapted their subsistence strategies to marine sources dropped from 13.3 to 6.3% in the caries frequencies, following

On the other hand, there are some exceptions about the correspondence between agriculture and caries. Several groups of modern farmers with a diet based almost exclusively on starch rich foods such as taro, sweet potato, and manioc, show low caries frequencies (Barmes et al., 1970; Baume 1969). In populations from Eastern Asia, the consumption of rice, despite their frequency, has produced low caries experiences (Tayles et al., 2000). Other especially high values of caries in populations with hunter-gatherers technology have been attributed to the consumption of cariogenic species traded with neighbor farmers17 (Lukacs, 1990;

17 African pigmies (Aka, Mbuti, Efe) traded meat and honey with the Bantu, who provided back manioc, maize, nuts, rice and plantains. In these hunter-gatherers honey is an important dietary source during

Nelson et al., 1999; Neves & Cornero, 1997; Pezo, 2010).

chamber exposure due to severe wear in anterior teeth.

the reduction in carbohydrates intake.

great part of the year (Walker & Hewlett, 1990).

Walker & Hewlett, 1990).

As we can see, the historical evaluation of caries allows us to recognize some trends and recurrences in prevalences, frequencies and patterns. Although in general it is possible to identify some critical variables such as the excessive consumption of refined sucrose or gelatinized starches as etiological agents, there are many other socio-historical factors, specific for each population, that must be considered before generalizing about the complex relationship between caries and subsistence pattern.
