**2. The antiquity of caries: Evidences of caries in hominines and early humans**

Caries is a very old disease and it is not exclusive of the human species. Evidences of dental lesions compatible with caries have been observed in creatures as old as Paleozoic fishes (570-250 million years), Mesozoic herbivores dinosaurs (245-65 million years), prehominines of the Eocene (60-25 million years), and Miocenic (25-5 million years), Pliocenic (5-1.6 million years), and Pleistocenic animals (1.6-0.01 million years – Clement, 1958; Kear, 2001; Kemp, 2003; Sala et al., 2004). Caries has also been detected in bears and other wild animals (Pinto & Exteberria, 2001; Palamra et al., 1981), and it is common in domestic animals (Gorrel, 2006; Shklair, 1981; Wiggs & Lobprise, 1997).

In humans, caries is one of the most widely spread diseases and its presence takes place into our species origins. Paleodietary reconstructions have provided a high amount of data on the presence of caries in ancestral lineages. An approximal groove located in the cementumenamel junction (CEJ) of bicuspids and molars has been noticed in several lineages of fossil hominines like Paranthropus robustus, *Homo habilis*, *H. erectus*, *H*. *heidelbergensis* and *H*. *neanderthalensis* (Bermúdez de Castro et al., 1997; Frayer, 1991; Milner & Larsen, 1991; Ungar et al., 2001). Although some scholars have reported that lesion as caries (Clement, 1956; Grine et al., 1990; Robinson, 1952), more recent analyses done in an specimen of *Homo erectus* from Olduvai Gorge (1.84 million years BP4) suggest that it could be an erosion produced by the habitual (possibly therapeutic) use of tooth-picks (Ungar et al., 2001).

Also, the paleopathological record of the ATE9-1 jaw (*Homo sp.* - Sima del Elefante site, Sierra de Atapuerca, Spain), considered the oldest hominine fossil of Western Europe (1.3 million years BP), shows numerous maxillary lesions such as hypercementosis, calculus deposits, periodontal disease, cystic lesions and an anomalous wear facet compatible with tooth picking but no caries (Martinón et al., 2011).

Several authors have suggested that the discovery of fire by *Homo erectus*-like species*,* around 800 thousand years ago, was a biologically significant step. Meanwhile cooked food replaced a

<sup>3</sup> Some prompts are used for the recording of caries experience. Caries prevalence, defined as the number of individuals in a population affected by caries in a specific time span. Caries frequency, defined as the number of teeth affected for caries divided by the total number of sockets observed (tooth/tooth socket) in a individual or population; and caries index as the Decay Missing Filling Index adapted to fragmentary samples (Duyar & Erdal, 2003; Lukacs, 1992; Medronho et al., 2009; Pezo, 2010; Saunders et al., 1997).

<sup>4</sup> The chronological dating methods use some conventional parameters. BP (before present) refers to a non- calibrated C14 date, calculated since 1950 as year zero. BC and AD (before Christ and *Anno Domini*  respectively) refers to a calibrated C14 date (calculated from accurate historical or geological data) in calendar years since the year one of our era (Taylor, 1987).

Considering the available data, we know that the highest caries rates3, their distribution and severity profiles observed nowadays are the result of a complex process of slow dietary changes, directly linked to the development of Western civilization. Consequently, the current caries patterns are not observed in past populations, on the opposite, they show a high variability along time and space that corresponds to a wide range of subsistence strategies,

Caries is a very old disease and it is not exclusive of the human species. Evidences of dental lesions compatible with caries have been observed in creatures as old as Paleozoic fishes (570-250 million years), Mesozoic herbivores dinosaurs (245-65 million years), prehominines of the Eocene (60-25 million years), and Miocenic (25-5 million years), Pliocenic (5-1.6 million years), and Pleistocenic animals (1.6-0.01 million years – Clement, 1958; Kear, 2001; Kemp, 2003; Sala et al., 2004). Caries has also been detected in bears and other wild animals (Pinto & Exteberria, 2001; Palamra et al., 1981), and it is common in domestic

In humans, caries is one of the most widely spread diseases and its presence takes place into our species origins. Paleodietary reconstructions have provided a high amount of data on the presence of caries in ancestral lineages. An approximal groove located in the cementumenamel junction (CEJ) of bicuspids and molars has been noticed in several lineages of fossil hominines like Paranthropus robustus, *Homo habilis*, *H. erectus*, *H*. *heidelbergensis* and *H*. *neanderthalensis* (Bermúdez de Castro et al., 1997; Frayer, 1991; Milner & Larsen, 1991; Ungar et al., 2001). Although some scholars have reported that lesion as caries (Clement, 1956; Grine et al., 1990; Robinson, 1952), more recent analyses done in an specimen of *Homo erectus* from Olduvai Gorge (1.84 million years BP4) suggest that it could be an erosion produced by

Also, the paleopathological record of the ATE9-1 jaw (*Homo sp.* - Sima del Elefante site, Sierra de Atapuerca, Spain), considered the oldest hominine fossil of Western Europe (1.3 million years BP), shows numerous maxillary lesions such as hypercementosis, calculus deposits, periodontal disease, cystic lesions and an anomalous wear facet compatible with

Several authors have suggested that the discovery of fire by *Homo erectus*-like species*,* around 800 thousand years ago, was a biologically significant step. Meanwhile cooked food replaced a

3 Some prompts are used for the recording of caries experience. Caries prevalence, defined as the number of individuals in a population affected by caries in a specific time span. Caries frequency, defined as the number of teeth affected for caries divided by the total number of sockets observed (tooth/tooth socket) in a individual or population; and caries index as the Decay Missing Filling Index adapted to fragmentary samples (Duyar & Erdal, 2003; Lukacs, 1992; Medronho et al., 2009; Pezo, 2010;

4 The chronological dating methods use some conventional parameters. BP (before present) refers to a non- calibrated C14 date, calculated since 1950 as year zero. BC and AD (before Christ and *Anno Domini*  respectively) refers to a calibrated C14 date (calculated from accurate historical or geological data) in

**2. The antiquity of caries: Evidences of caries in hominines and early** 

specific cultural regulations, and particular historical processes.

animals (Gorrel, 2006; Shklair, 1981; Wiggs & Lobprise, 1997).

the habitual (possibly therapeutic) use of tooth-picks (Ungar et al., 2001).

tooth picking but no caries (Martinón et al., 2011).

calendar years since the year one of our era (Taylor, 1987).

**humans** 

Saunders et al., 1997).

diet entirely based on raw meat and vegetables, the patterns of chewing, digestion and nutrition changed accordingly. The process of cooking using fire turned the food safer, juicer, and easier to digest, promoting a higher intake of energy that, in evolutionary terms, had a sequence of favorable physiological effects. The easy digestion of cooked food would have favored the reduction of the digestive system, facilitating metabolic energy savings that were used to develop the brain (Aiello & Wheeler, 1995; Cartmill, 1993; Wrangham, 2009). Nevertheless, it is supposed that *H. erectus,* a hunter-gatherer, obtained approximately 50% of its calories from carbohydrates (Wrangham, 2009) and under the hypothesis of cooking (that obviously included meat and vegetables), caries should have been present much earlier in the fossil record. However, caries appears clearly much later. So, the data on oral does not support the idea of a cariogenic diet based on cooked vegetables from the earliest periods. Maybe, in the beginning, fire was employed only for cooking meat.

The unquestionable oldest evidence of caries comes from a fossil found in 1921 in Broken Hill, Northern Rhodesia (Zambia) during the exploration of a zinc mine. The specimen denominated Broken Hill 1, a *Homo rhodesiensis* cranium (African version of the *Homo heidelberguensis*  650,000-160,000 BP) shows extensive dental caries and coronal destruction. Except for five teeth, all the rest is affected by rampant caries and several crowns are almost completely destroyed. Caries seems to have its origin in the interdental spaces. Besides, Broken Hill man experienced alveolar recession and dental abscesses in many teeth (Fig. 1). Although lesions have been attributed to a diet rich in vegetables and/or poisoning by the existing metals in the region (Bartsiokas & Day, 1993), it seems that, given the interdental origin of the caries and the absence of tooth picks evidence, the Broken Hill 1 developed his lesions due to his ignorance in the use of tooth picks, which was known by other earlier hominines (Puech, 1978).

Fig. 1. **The unquestionable oldest evidence of caries in the human paleontological record.**  Pictures of *H. rhodesiensis* skull cast. Map modified from Google Maps 2010.

Caries Through Time: An Anthropological Overview 7

Dental caries are present but still rare among early modern humans (European and Near Eastern *Homo sapiens*) during the Upper Paleolithic. Caries have been identified in Qafzeh 3 and Skhul 2 in Israel (Fryer, 1976; Boydstun et al., 1988), and only Cro-Magnon 4, Les Rois R50-4 and Les Rois R51-15 have been indentified with caries in Europe (Brennan, 1991; Trikanus et al., 2000). Caries are more widely found among more recent Eurasian foraging

peoples, but caries frequencies remain below 10% (Brothwell, 1963; Caselitz, 1998).

**3.1 Dietary changes and the raise of caries experience in past human societies** 

(Hillson, 2001; Lukacs, 1992; Powell, 1985; Turner, 1979).

In fact, the history of dental caries is associated with the rise of civilization, and more recently with dietary changes that occurred since the Mercantilism and Industrial Revolution. Several archaeological and historical works have confirmed the relationship between high caries frequencies and prevalences and the increase of carbohydrates intake in human populations from the advent of agriculture6 (Larsen, 1997; Saunders et al., 1997; Turner, 1979). Generally hunter-gatherers show low caries frequencies whereas peoples based on mixed economies, gardening, and farming, show increasingly higher caries rates

For instance, in the North American Southeast the number of carious teeth in farmers is three times the number of carious teeth in foragers of prior epochs (Powell, 1985). In several populations from Eastern Woodlands of North America the changes are also observed along the time, with frequencies below 7% in Archaic foragers and frequencies over 15% in farmer's phases contemporary to the first contact with Europeans (Larsen, 1997). In prehistoric peoples from Colombia, the prevalence of caries is close to zero in huntergatherers that used lithic technology, appears in early farmers and increases in potterymakers, reaching frequencies of up to 76% (Rodríguez, 2003). These same tendencies have been observed in native modern peoples that had their traditional diets replaced by western

ones, during the process of global colonization (Holloway et al., 1963; Mayhall, 1970).

Caselitz (1998) analyzed the historical evolution of caries in 518 human populations of Europe, Asia and America in a wide timeline from the Paleolithic to the present, confirming that during Paleolithic and Mesolithic periods, the hunter-gatherers had less caries and lesions progressed more slowly. Caries indices have increased gradually from Neolithic times, until they reach the high rates observed at the present. Considering only the Holocene (the last 10,000 BC) in the Old World, he observed that the low indices7 of Mesolithic times remain relatively constant during the Early Neolithic (between the 9th and 5th millennium

6 Agriculture is a set of knowledge and techniques aimed to control the natural environment for production of crops. The transition from the hunting-gathering economy to self-sufficient food production changed radically the human history, promoting a high population growth for food availability, sedentary settlements, new labor division, and changes in the rights of land property that led to a more complex society, with specialists, social classes and centralized government systems. 7 For his comparisons, Caselitz used a reduced variant of the DMF Index (Decayed Missing Filling Index) applied to archaeological samples, the I-CE (Index of carie-extractio) or DMI (Decay Missing Index – Lukacs, 1996; Pezo & Eggers, 2010; Saunders et al., 1997), calculated as the number of carious teeth added to the number of antemortem toot loss (AMTL) divided by the sum of teeth and sockets

**3. Caries and lifestyle** 

observed.

In this sense, from the presence of caries in non-human primates one must consider that natural sources of carbohydrates can produce carious lesions. Caries have been reported in prime-age individuals of *Pongo pygmaeus* (4.1%), *Gorilla gorilla* (2.7%), *Hylobates* (0.9%) and *Pan troglodytes* (12.7% in juveniles versus 30.6% in older animals – Crovella & Ardito, 1994; Schultz, 1956). Thus, in modern apes, the disease exists despite them being mostly herbivorous with a raw diet based on only a few starchy tubers if any (Kilgore, 1995; Miles & Grigson, 1990).

The Neanderthals (230,000-30,000 BP) show a high prevalence of enamel hypoplasias, antemortem tooth loss, periodontal disease and abscesses but dental caries is very rare among them (Brennan, 1991; Brothwell, 1963; Grine et al., 1990; Ogilvie, 1989). Six cases (Table 1) of dental caries (0.48%) have been reported among the approximately 1250 known Neanderthal teeth (Lalueza et al., 1993; Lebel & Trinkaus, 2001; Tillier et al., 1995; Trinkaus et al., 2000; Walker et al., 2011). The presence of caries in Neanderthals suggests the existence of pathogenic dental plaque and dietary conditions compatible with the consumption of some cariogenic carbohydrates despite the hunter-gatherer lifestyle and cold climate existing during the Middle Paleolithic5 (Trinkaus et al., 2000).


Table 1. Carious lesions among Neanderthals

<sup>5</sup> The Paleolithic or Antique Stone Age was the longest period of human prehistory (99% of it), ranging from 2.8 millions of years (in Africa) to 10,000 BP. The Paleolithic is divided in three periods: Lower Paleolithic (2.8 million years to 200,000 years: the epoch of the hominines and our first ancestors), Middle Paleolithic (the epoch of Neanderthals, from approximately 200,000 to 30,000 BP), and Upper Paleolithic (30,000 BP- 10,000 BP – the epoch of the earliest modern humans). The Neolithic or New Stone Age was defined considering the new way of life based on the production of food from domesticated species. It appears at different times and regions around the world during the Holocene (starts 10,000 BP). The phase of transition between the Paleolithic and Neolithic is known as Mesolithic (Carbonell, 2005).

Dental caries are present but still rare among early modern humans (European and Near Eastern *Homo sapiens*) during the Upper Paleolithic. Caries have been identified in Qafzeh 3 and Skhul 2 in Israel (Fryer, 1976; Boydstun et al., 1988), and only Cro-Magnon 4, Les Rois R50-4 and Les Rois R51-15 have been indentified with caries in Europe (Brennan, 1991; Trikanus et al., 2000). Caries are more widely found among more recent Eurasian foraging peoples, but caries frequencies remain below 10% (Brothwell, 1963; Caselitz, 1998).

### **3. Caries and lifestyle**

6 Contemporary Approach to Dental Caries

In this sense, from the presence of caries in non-human primates one must consider that natural sources of carbohydrates can produce carious lesions. Caries have been reported in prime-age individuals of *Pongo pygmaeus* (4.1%), *Gorilla gorilla* (2.7%), *Hylobates* (0.9%) and *Pan troglodytes* (12.7% in juveniles versus 30.6% in older animals – Crovella & Ardito, 1994; Schultz, 1956). Thus, in modern apes, the disease exists despite them being mostly herbivorous with a raw diet based on only a few starchy tubers if any (Kilgore, 1995; Miles

The Neanderthals (230,000-30,000 BP) show a high prevalence of enamel hypoplasias, antemortem tooth loss, periodontal disease and abscesses but dental caries is very rare among them (Brennan, 1991; Brothwell, 1963; Grine et al., 1990; Ogilvie, 1989). Six cases (Table 1) of dental caries (0.48%) have been reported among the approximately 1250 known Neanderthal teeth (Lalueza et al., 1993; Lebel & Trinkaus, 2001; Tillier et al., 1995; Trinkaus et al., 2000; Walker et al., 2011). The presence of caries in Neanderthals suggests the existence of pathogenic dental plaque and dietary conditions compatible with the consumption of some cariogenic carbohydrates despite the hunter-gatherer lifestyle and

cold climate existing during the Middle Paleolithic5 (Trinkaus et al., 2000).

Maxillary I2

Maxillary M1 or M2

Mandibular dm1

5 The Paleolithic or Antique Stone Age was the longest period of human prehistory (99% of it), ranging from 2.8 millions of years (in Africa) to 10,000 BP. The Paleolithic is divided in three periods: Lower Paleolithic (2.8 million years to 200,000 years: the epoch of the hominines and our first ancestors), Middle Paleolithic (the epoch of Neanderthals, from approximately 200,000 to 30,000 BP), and Upper Paleolithic (30,000 BP- 10,000 BP – the epoch of the earliest modern humans). The Neolithic or New Stone Age was defined considering the new way of life based on the production of food from domesticated species. It appears at different times and regions around the world during the Holocene (starts 10,000 BP). The phase of transition between the Paleolithic and Neolithic is known as Mesolithic

**Specimen Tooth Description** 

Mandibular M3 Two small pits with irregular shapes in

Maxillary dm1 A mid-lingual pit lesion.

MandibularM2 A small interproximal notch.

occlusal fissures, penetration beyond the dento-enamel junctions.

A cavity in the central pit of a strongly shoveled tooth, 2.6 mm diameter, extended through the dento-enamel junction.

A large hole across the disto-lingual corner of the cervical half of the roots, 7.2 mm high, 6.3 mm wide, 3.5 mm depth.

An occlusal cavity, 1.2 mm diameter, extended through the exposed dentin.

& Grigson, 1990).

Banyoles 1 France (Lalueza et al., 1993).

Kebara 27 Israel (Tillier et al., 1995)

Bau de l'Aubesier 5 France (Trinkaus et al., 2000)

Bau de l'Aubesier 12 France (Lebel &Trinkaus, 2001)

Sima de Palomas 25 Spain (Walker et al., 2011)

Sima de Palomas 59 Spain (Walker et al., 2011)

(Carbonell, 2005).

Table 1. Carious lesions among Neanderthals

#### **3.1 Dietary changes and the raise of caries experience in past human societies**

In fact, the history of dental caries is associated with the rise of civilization, and more recently with dietary changes that occurred since the Mercantilism and Industrial Revolution. Several archaeological and historical works have confirmed the relationship between high caries frequencies and prevalences and the increase of carbohydrates intake in human populations from the advent of agriculture6 (Larsen, 1997; Saunders et al., 1997; Turner, 1979). Generally hunter-gatherers show low caries frequencies whereas peoples based on mixed economies, gardening, and farming, show increasingly higher caries rates (Hillson, 2001; Lukacs, 1992; Powell, 1985; Turner, 1979).

For instance, in the North American Southeast the number of carious teeth in farmers is three times the number of carious teeth in foragers of prior epochs (Powell, 1985). In several populations from Eastern Woodlands of North America the changes are also observed along the time, with frequencies below 7% in Archaic foragers and frequencies over 15% in farmer's phases contemporary to the first contact with Europeans (Larsen, 1997). In prehistoric peoples from Colombia, the prevalence of caries is close to zero in huntergatherers that used lithic technology, appears in early farmers and increases in potterymakers, reaching frequencies of up to 76% (Rodríguez, 2003). These same tendencies have been observed in native modern peoples that had their traditional diets replaced by western ones, during the process of global colonization (Holloway et al., 1963; Mayhall, 1970).

Caselitz (1998) analyzed the historical evolution of caries in 518 human populations of Europe, Asia and America in a wide timeline from the Paleolithic to the present, confirming that during Paleolithic and Mesolithic periods, the hunter-gatherers had less caries and lesions progressed more slowly. Caries indices have increased gradually from Neolithic times, until they reach the high rates observed at the present. Considering only the Holocene (the last 10,000 BC) in the Old World, he observed that the low indices7 of Mesolithic times remain relatively constant during the Early Neolithic (between the 9th and 5th millennium

<sup>6</sup> Agriculture is a set of knowledge and techniques aimed to control the natural environment for production of crops. The transition from the hunting-gathering economy to self-sufficient food production changed radically the human history, promoting a high population growth for food availability, sedentary settlements, new labor division, and changes in the rights of land property that led to a more complex society, with specialists, social classes and centralized government systems.

<sup>7</sup> For his comparisons, Caselitz used a reduced variant of the DMF Index (Decayed Missing Filling Index) applied to archaeological samples, the I-CE (Index of carie-extractio) or DMI (Decay Missing Index – Lukacs, 1996; Pezo & Eggers, 2010; Saunders et al., 1997), calculated as the number of carious teeth added to the number of antemortem toot loss (AMTL) divided by the sum of teeth and sockets observed.

Caries Through Time: An Anthropological Overview 9

recent periods of Modern Age, almost 60% of individuals were affected, and in contemporary times the observations denote global values surpass 95% (Nikiforouk, 1985; Rugg-Gunn & Hackett, 1993; Shafer et al., 1983). These trends have been pointed out in

In the American continent caries has been recorded since approximately 7000 BC with relatively high indices that decrease around 5000 BC (Bernal et al., 2007; Caselitz, 1998). A dramatic increase was noticed since 2300 BC. Although we do not have complete dietary inventories for each different period, the high caries rates of the oldest Americans could be related to the consumption of endemic fruits rich in maltodextrines and sugar, such as carob (*Prossopis sp.*) and acacia (*Acacia sp.*). This decrease could be explained by a reorientation in the subsistence activities that turned to marine foraging during the Middle Holocene (around 6000 BP), whereas the highest peak can be clearly related with the summit of

Fig. 2. **Caries trends in the Old World across time.** a) Indus valley civilization sequence, caries frequency versus corrected frequency (Lukacs, 1996). b) Britain sequence, caries

frequency versus prevalence (Roberts & Cox, 2007).

other studies (Moore & Corbet, 1971, 1973, 1975; Roberts & Cox, 2007 – Fig. 2b).

agricultural production.

BC), but suffered a dramatic increase of 75% in a short time span of few centuries around 4500 BC. This phenomenon, observed in North Africa, Near East, China and Europe has been attributed to the drastic change in the diet that means the introduction and spread of cereals in the entire antique world (Caselitz, 1998).

In the Mediterranean region, Arabia and India the increase of caries began early between the 7th and 5th millennium BC. In Natufians from the Levant region, the phase of huntergatherers (10,500-8300 BC) shows 6.4% of caries frequency whereas Neolithic populations (8300-5500 BC) show 6.7% (Eshed et al., 2006). In the Indo region the caries frequencies range between 1.4-1.8% in the earliest populations, but in the site of Harappa (5000 BP, Pakistan) from the Early Bronze Age8 the caries frequency is 12% (Lukacs, 1992, 1996) whereas an Iron Age skeletal sample from Oman shows 32.4% (Nelson & Lukacs, 1994) analyzed under the same methods (Fig. 2a). During the Chinese Neolithic, the initial phase Yangshao (7000 – 5000 BP) shows rare evidence of caries (0.04%) and all of them occur in the posterior sector of the mouth. The Longshan period (4500 – 4000 BP) presents caries frequencies of 0.30% and besides, showing caries located in the anterior teeth. The Chinese farming in this epoch was based on domesticated species of millet (*Setaria italica*), broomcorn millet (*Panicum miliaceum*) and rice (*Oryza sativa* – Pechenkina et al., 2002)*.*

The most antique written reference of oral diseases in this region comes from a tablet of clay with cuneiform inscriptions from the lower valley of the Euphrates dated at 5000 BC. The tablet refers to the existence of a "worm" responsible for tooth pain and a recipe for spelling it. More than 3000 years later, in Egypt, the Eber's papyrus, a kind of medical tractate dated around 1550 BC, refers to the existence of gingivitis, pulpitis and dental pain and their treatment using dressings, mouth washers and enchantments (Nikiforouk, 1985). In antique civilizations caries and antemortem teeth loss seemed to be a permanent scourge that obviously must have caused the same physical and psychological suffering it causes nowadays. The first attempts of restorative dentistry have been recorded in Egyptians, Phoenicians, Etruscans and Romans (Asbell, 1948; Harris et al., 1975; Jackson, 1988; Puech, 1995; Teschler-Nichola et al., 1998).

In Europe caries rates are almost stable during the Middle Bronze Age (1600-1200 BC) and increase continuously between 1200 BC and 500 AD. It could mean that the spread of agriculture occurred at least one millennium later than in other Old World regions. A little peak is observed around 750 AD followed by a phase relatively stable during the Middle Age and a second increase, much more dramatic, is observed since the 16th century, and it has reached the highest records in our times (Caselitz, 1998). Examining the proportion of affected individuals per population, Caselitz (1998) observed that during the fifth millennium BC, around one third of individuals were affected with caries. In the Middle and Late Bronze Age (1500-300 BC) the affected proportion of individuals decreases relatively and then rose dramatically to 56% in the 7th century AD. This condition of deterioration remains constant until around 1300 AD when it reaches a new peak. In more

<sup>8</sup> In 1820, Christian Thomsen classified the prehistory of Europe in three ages (Cooper Age or Chalcolithic, Bronze Age and Iron Age) based on the analysis of metallic artifacts. Bronze Age was divided into Antique, Middle and Final Bronze Age but dates are different according to the region analyzed. In the Near East bronze appears at the final of the 4th millennium BC, in Greece around 2500 BC, in Persia in 2000 BC, and only about 1800 BC in China (Lull et al., 1991).

BC), but suffered a dramatic increase of 75% in a short time span of few centuries around 4500 BC. This phenomenon, observed in North Africa, Near East, China and Europe has been attributed to the drastic change in the diet that means the introduction and spread of

In the Mediterranean region, Arabia and India the increase of caries began early between the 7th and 5th millennium BC. In Natufians from the Levant region, the phase of huntergatherers (10,500-8300 BC) shows 6.4% of caries frequency whereas Neolithic populations (8300-5500 BC) show 6.7% (Eshed et al., 2006). In the Indo region the caries frequencies range between 1.4-1.8% in the earliest populations, but in the site of Harappa (5000 BP, Pakistan) from the Early Bronze Age8 the caries frequency is 12% (Lukacs, 1992, 1996) whereas an Iron Age skeletal sample from Oman shows 32.4% (Nelson & Lukacs, 1994) analyzed under the same methods (Fig. 2a). During the Chinese Neolithic, the initial phase Yangshao (7000 – 5000 BP) shows rare evidence of caries (0.04%) and all of them occur in the posterior sector of the mouth. The Longshan period (4500 – 4000 BP) presents caries frequencies of 0.30% and besides, showing caries located in the anterior teeth. The Chinese farming in this epoch was based on domesticated species of millet (*Setaria italica*),

broomcorn millet (*Panicum miliaceum*) and rice (*Oryza sativa* – Pechenkina et al., 2002)*.*

The most antique written reference of oral diseases in this region comes from a tablet of clay with cuneiform inscriptions from the lower valley of the Euphrates dated at 5000 BC. The tablet refers to the existence of a "worm" responsible for tooth pain and a recipe for spelling it. More than 3000 years later, in Egypt, the Eber's papyrus, a kind of medical tractate dated around 1550 BC, refers to the existence of gingivitis, pulpitis and dental pain and their treatment using dressings, mouth washers and enchantments (Nikiforouk, 1985). In antique civilizations caries and antemortem teeth loss seemed to be a permanent scourge that obviously must have caused the same physical and psychological suffering it causes nowadays. The first attempts of restorative dentistry have been recorded in Egyptians, Phoenicians, Etruscans and Romans (Asbell, 1948; Harris et al., 1975; Jackson, 1988; Puech,

In Europe caries rates are almost stable during the Middle Bronze Age (1600-1200 BC) and increase continuously between 1200 BC and 500 AD. It could mean that the spread of agriculture occurred at least one millennium later than in other Old World regions. A little peak is observed around 750 AD followed by a phase relatively stable during the Middle Age and a second increase, much more dramatic, is observed since the 16th century, and it has reached the highest records in our times (Caselitz, 1998). Examining the proportion of affected individuals per population, Caselitz (1998) observed that during the fifth millennium BC, around one third of individuals were affected with caries. In the Middle and Late Bronze Age (1500-300 BC) the affected proportion of individuals decreases relatively and then rose dramatically to 56% in the 7th century AD. This condition of deterioration remains constant until around 1300 AD when it reaches a new peak. In more

8 In 1820, Christian Thomsen classified the prehistory of Europe in three ages (Cooper Age or Chalcolithic, Bronze Age and Iron Age) based on the analysis of metallic artifacts. Bronze Age was divided into Antique, Middle and Final Bronze Age but dates are different according to the region analyzed. In the Near East bronze appears at the final of the 4th millennium BC, in Greece around 2500

BC, in Persia in 2000 BC, and only about 1800 BC in China (Lull et al., 1991).

cereals in the entire antique world (Caselitz, 1998).

1995; Teschler-Nichola et al., 1998).

recent periods of Modern Age, almost 60% of individuals were affected, and in contemporary times the observations denote global values surpass 95% (Nikiforouk, 1985; Rugg-Gunn & Hackett, 1993; Shafer et al., 1983). These trends have been pointed out in other studies (Moore & Corbet, 1971, 1973, 1975; Roberts & Cox, 2007 – Fig. 2b).

In the American continent caries has been recorded since approximately 7000 BC with relatively high indices that decrease around 5000 BC (Bernal et al., 2007; Caselitz, 1998). A dramatic increase was noticed since 2300 BC. Although we do not have complete dietary inventories for each different period, the high caries rates of the oldest Americans could be related to the consumption of endemic fruits rich in maltodextrines and sugar, such as carob (*Prossopis sp.*) and acacia (*Acacia sp.*). This decrease could be explained by a reorientation in the subsistence activities that turned to marine foraging during the Middle Holocene (around 6000 BP), whereas the highest peak can be clearly related with the summit of agricultural production.

Fig. 2. **Caries trends in the Old World across time.** a) Indus valley civilization sequence, caries frequency versus corrected frequency (Lukacs, 1996). b) Britain sequence, caries frequency versus prevalence (Roberts & Cox, 2007).

Caries Through Time: An Anthropological Overview 11

(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).

span of eight centuries, no significant changes in diet occurred (Vodanovic et al., 2005).

Varrela, 1991; Vodanovic et al., 2005; Watt et al., 1997).

Columbus in 1493 (Bernstein, 2009; Parker, 2011).

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;

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

10 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

11 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).

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

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