The antiquity of caries Evidences of caries in hominines and early humans

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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), pre-hominines 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 cementum-enamel 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 (Bermudez 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 (Martinon 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

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; Saunders et al., 1997).

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

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.

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.

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).

Specimen

Tooth

Description

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

Mandibular M3

Two small pits with irregular shapes in occlusal fissures, penetration beyond the dento-enamel junctions.

Kebara 27 Israel (Tillier et al., 1995)

Maxillary I2

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

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

Maxillary dm1

A mid-lingual pit lesion.

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

Maxillary M1 or M2

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.

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

Mandibular dm1

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

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

MandibularM2

A small interproximal notch.

Table 1. Carious lesions among Neanderthals

Table 1. Carious lesions among Neanderthals

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 (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).

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