It has long been recognised that the skulls of our hunter-gatherer forebears possessed much healthier teeth and dental structure than those of the agriculturalists that followed. The recent discovery that dental plaque contains DNA from ancient oral microbes is providing new evidence about the dietary patterns responsible for these changes.
Understanding the dietary habits of our paleolithic ancestors can shed light on which contemporary foods might best match our genetic constitution. A recent edition of New Scientist (19/04/14, p50)  carried an excellent article about the work of Alan Cooper and his team of the Australian Centre for Ancient DNA. They have analysed genetic material traped in dental plaque from skulls spanning the late paleolithic (hunter-gatherer), neolithic (farming), right up to modern industrial man .“Hunter-gatherers had really good teeth,” says Alan Cooper “[But] as soon as you get to farming populations, you see this massive change. Huge amounts of gum disease. And cavities start cropping up.”
The idea that you can extract microbial DNA from plaque is new as DNA rarely survives decay and fossilisation. Microbes in the gut, and in faeces, decay rapidly after the death of the host, before fossilisation takes place. Until recently, no one guessed that such genetic material could be preserved so effectively in plaque. Fortunately our ancient ancestors were not big on dental hygiene. Layers of calcified plaque built up over their lifetime, effectively fossilising oral bacteria in the plaque’s cement-like matrix. So Cooper’s team were able to analyse the microbial DNA from skulls with plaque intact and begin to build up a picture of how and why the microbiome has changed. Their work is especially important as an inflammatory gut flora, where pathogenic bacteria come to dominate the gastrointestinal tract, has been linked to modern diseases such as gum disease, diabetes, heart disease and asthma. With these diseases increasing globally as developing nations adopt a westernised lifestyle and diet, it becomes all the more urgent to understand the influence of our gut microbes on health.
So what did Coopers team find?
Two species that changed dramatically are shown in the graph opposite. Firstly, streptococus mutans, the bacteria commonly considered responsible for tooth decay, appeared in humans’ oral cavity in the Neolithic period, coinciding with a change to agricultural diets. Furthermore, they found it increased dramatically as refined sugars became prevalent from the industrial revolution onwards, confirming the long-held idea among dental researchers that sugar along with this particular species, are the primary cause of tooth decay.
“Our carbohydrate rich diet has transformed our oral ecosystems for the worse”
Another bacteria, responsible for gum disease is porphyromonas gingivalis, and it too increased dramatically once farming began at the start of the Neolithic.
“Like cavities, gum disease seems to have set in when peoples began farming”
Researchers now link these altered microbiomes to a range of diseases. For example periodontitis (inflammation around the tooth) will affect 13% of americans at some point in their lifetime. The relevance of this disease extends beyond the mouth. Diabetes has been linked to inflammation caused when oral microbes interact with the immune system. Furthermore, although the jaw has a specialised immune system (New Scientist, 20/11/05)  to deal with oral bacteria that manage to get into the blood, recent studies have found that some oral microbes not only gain entry to the blood stream, but can form plaques that block arteries, extending the link between dental and systemic health problems.
“You’re walking around with a permanent immune response, which is not a good thing,” says Cooper. “It causes problems all over the place.”
It has commonly been assumed that the reason for paleolithic hominids excellent immunity to tooth decay was because their diets were rich in meat, and low in sugar. However, the New Scientist article reports that Alan Cooper’s team question the simplicity of this idea, suggesting that their oral microbiome simply did not contain the modern cariogenic strains (those that cause dental caries) that arose with the switch to farming. They cite evidence that Neanderthals living in the middle east 28,000 years ago ate a lot of sugary dates, but did not suffer dental disease. On the face of it this makes a lot of sense, and suggests that it was not so much the diet as the oral microbes which protected their teeth. This fits with the dominant idea in dentistry of caries as an infectious disease, but makes it harder to explain what it was about the agricultural diet that lead to such a large change in dental health. At this point we need to consider some contradictory data that the New Scientist article did not cover.
Firstly, whilst sugary sticky fruits like dates, raisins and sultanas appear to be the perfect medium for promoting tooth decay, this has been shown not to be the case. For caries to start three things are needed: low oral pH (acidic), food sticking to teeth and bacteria that can turn the sugar into acids that attack enamel. In 2013 Wong et al.  reviewed the available studies and concluded that:
.. consumption [of raisins] alone does not drop oral pH below the threshold that contributes to enamel dissolution, do not remain on the teeth longer than other foods, and contain a variety of antioxidants that inhibit Streptococcus mutans, bacteria that is a primary cause of dental caries.
So perhaps those date-eating-Neanderthals would not have been at risk anyway. Also, we should bear in mind that dates are a seasonal fruit, only available for a few months of the year. (Unless Neanderthals had learned to dry and thereby preserve their dates, but this doesn’t seem likely as archaeologists have not found any little wooden boxes!)
A second challenge to the New Scientist’s conclusions come from considering whether the detrimental change to oral health associated with Neolithic farming were caused by an increased consumption of starches rather than sugars.
Paleolithic tooth decay
Earliest evidence for caries and exploitation of starchy plant foods in Pleistocene hunter-gatherers from Morocco, Louise T. Humphrey et al. PNAS, 2013 
Tooth decay among pre-agricultural hunter gatherers is certainly the exception not the rule, so where it arises we can potentially learn a lot about the causes. The photo above shows severe tooth decay in paleolithic skulls from Morocco, c. 14,000 years ago. This is direct evidence that in rare conditions, caries did happen in pre-agricultural humans. Isabelle De Groote, who studied the teeth, said:“These people’s mouths were often affected by both cavities in the teeth and abscesses, and they would have suffered from frequent toothache.”
So what were they eating? Excavations of burial areas showed evidence of methodical harvesting and processing of wild foods, including sweet acorns, pine nuts and land snails. It is primarily the starchy acorns that have been implicated in the tooth decay. The authors conclude:
“We infer that increased reliance on wild plants rich in fermentable carbohydrates caused an early shift toward a disease-associated oral microbiota.”
So it seems to be the starches, rather than fruit sugar, that are behind disbiosis leading to tooth decay, and indicates two key points: Typical paleolithic diets were probably low in starches, but may have included seasonal fruits. The explosion in widespread dental problems associated with the switch to farming can likely be attributed to the increase in starch consumption.
Modern dentistry has come to a similar conclusion, that tooth decay is stimulated more by starchy foods more than sugar. Because sugar (especially sucrose) is metabolised to lactic acid by streptococus mutans this microorganism has been considered a causal agent in tooth decay, effectively treating caries as an infection. But ideas are changing. A 2013 paper in International Dental Journal , questions the idea that s. mutans is the sole cause of tooth decay.
While simple sugars can be cariogenic, cooked starches are also now recognised to be a caries threat, especially because such starches, while not ‘sticky in the hand’, can be highly retentive in the mouth. Metabolism of starch particles can yield a prolonged acidic challenge, especially at retentive, caries-prone sites… …Preventing the transmission of S. mutans will likely be inadequate to prevent caries if a sufficiently carbohydrate-rich diet continues. Similarly, restriction of sucrose intake, although welcome, would be unlikely to be a panacea for caries, especially if frequent starch intake persisted.
Taken together these studies indicate that a starch based diet is sub-optimal for humans, and that the neolithic decline in dental health may best be attributed to increased starch consumption. The only problem with this conclusion is that you can find hunter gatherer populations that eat (or ate) a diet relatively high in starches, such as the pygmy of Africa  who show low levels of caries. Furthermore, some primitive agriculturalists such as the Kitavans , who’s staple diet is based around starchy roots such as of yam, sweet potato, cassava, taro along with fish, have excellent dental health and are famed for living to old age with none of the diseases of civilisation.
So where does that leave us? Starches have been implicated in the health problems associated with the advent of agriculture, yet we have examples of traditional diets based on starches from underground storage organs (tubers) that do not induce dental decay. The only starches left to consider are those from grains, and grains more than any other food mark out the dietary shift associated with the neolithic transition. In terms of human evolution, grains were a completely novel staple food. So what is the evidence that grains are linked to dental decay?
Drs Edward and May Mellanby, 1932
The Mellanby’s were famous in their time for spearheading the eradication of rickets which was endemic in Europe in the early 20th century. Their discovery of vitamin D as a cure for rickets effectively eliminated this disease, and made them household names. However, they are less well-known for their pioneering work on caries.
In 1932 they demonstrated the reversal of dental caries  in children through dietary modification. The 6 month investigation was sponsored by the UK Medical Health Council at the request of the Dental Disease Committee. These were serious public bodies attempting to understand the causes of tooth decay which was a widespread public health issue. The Mellanbys demonstrated that caries could not only be reduced, but reversed by providing a diet with:
- Increased Calcium and Phosphorus from milk
- Sufficient Vitamin D from sunlight or animal foods
- A significant reduction in cereal grains (not sugar)
Here are the results of their six month trial, comparing three dietary regimens on the progress of caries in children:
Only with the elimination of grains from the diet did the children’s teeth heal. So why would grains produce such a negative effect on tooth development in children?
Part of the answer is the fact that grains contain phytates, a class of phosphate bearing compounds found in many seeds (especially grains and nuts), that bind to dietary calcium, zinc and iron. In humans phytates reduce the absorption of these minerals , which can be critical in the growth of bones and teeth, especially during childhood. If the proper mineralisation of teeth is retarded during development then those teeth remain more vulnerable to caries throughout life. Another problem with grains is that they tend to be low in calcium, zinc and iron in the first place, so diets heavily dependent on grains tend to lead to deficiency in these important minerals.
Other seeds, including many nuts, also contain high levels of phytates. This may explain why the late paleolithic North African acorn-eaters suffered levels of dental decay usually only found in agriculturalists, whilst the low-phytate diet associated with the Middle Eastern date-eating Neanderthals enabled them to escape caries.
Further, the damaging effects of grains go deeper than just the teeth, affecting the development of the skeleton in multiple ways. For example, grains in childhood can reduce calcium levels sufficiently to contribute to rickets . Cases of rickets have increased in the UK and other developed countries in recent years, and there have been notable cases amongst children of vegetarian parents . Those raised on a macrobiotic diet (very high in whole grains) are at an even greater risk of deficiencies . Yet whilst it would appear that grains have a negative impact on bone and teeth health, meat consumption may have a protective effect against rickets . This last point may explain the absence of rickets among traditional Eskimo who subsisted on a diet high in animal products at latitudes where vitamin D synthesis would have been seriously limited. The excellent dental health of the traditional Eskimo is attested to by Weston Price, who in the 1930s documented how rapidly dental problems increased once they switched to western dietary patterns .
Grains have also been implicated in Porotic Hyperostosis and Cribra Orbitalia – bone disorders associated with insufficient iron absorption. These conditions interests archaeologists as they appear in the fossil record of peoples with a high dependency on grains. Jess Beck, a PhD candidate in anthropology explains
It has long been acknowledged that the frequency of porotic hyperostosis increases regionally with the adoption of agriculture. In addition to being poor sources of iron themselves, cereal grains like maize contain phytic acid, which has a deleterious effect on the ability of the intestine to absorb dietary iron.
Putting all of the above together, evidence from ancient human teeth seems to indicate that humans are maladapted to consumption of seeds (especially grains) which are implicated in a range of dental and skeletal problems, and are linked to an inflammatory oral dysbiosis, which itself is linked to the diseases of civilisation.
- DNA analysis of dental plaque shows that the modern oral microbiome is pro-inflammatory and cariogenic
- It shows that this dysbiosis began with the Neolithic advent of farming
- Starchy foods, more than sugary fruits, are associated with dental caries even in pre-agrcultural populations suggesting that they may be cariogenic with or without oral dysbiosis
- Seed starches (grains) are implicated in a range of dental and skeletal problems rather than starchy tubers
So what can we do?
Alan Cooper says:
“We brush our teeth and we floss, and we think that we’ve got good oral hygiene. But [we’re] completely failing to deal with the underlying problem. Ten years from now, I think we’re going to find that the whole microbiome is a key part of what you get monitored for and treated for.”
Cooper suggests that one way to help return our oral microbiome to a healthier, more balanced state might be to cut out processed carbohydrates and start eating like our ancestors. That makes sense to me!
 Pearly time capsule. Sharon Levy, New Scientist, p50-53, 19/04/2014
The discovery that fossilised teeth are bursting with ancient microbial DNA sheds new light on the lives of our ancestors and our own health
 Sequencing ancient calcified dental plaque shows changes in oral microbiota with dietary shifts of the Neolithic and Industrial revolutions Christina J Adler et al. Nature Genetics, Feb 2013
Two of the greatest dietary shifts in human evolution involved the adoption of carbohydrate-rich Neolithic (farming) diets (beginning ~10,000 years before the present) and the more recent advent of industrially processed flour and sugar (in ~1850)
 Why a loose tooth needn’t mean a sore jaw New Scientist, 20/11/2005
 Raisins and oral health Wong et al, Journal of Food Science, Jun 2013
 Earliest evidence for caries and exploitation of starchy plant foods in Pleistocene hunter-gatherers from Morocco, Louise T. Humphrey et al. PNAS, 2013
Macrobotanical remains from occupational deposits dated between 15,000 and 13,700 cal B.P. provide evidence for systematic harvesting and processing of edible wild plants, including acorns and pine nuts. Analysis of oral pathology reveals an exceptionally high prevalence of caries (51.2% of teeth in adult dentitions), comparable to modern industrialized populations with a diet high in refined sugars and processed cereals. We infer that increased reliance on wild plants rich in fermentable carbohydrates and changes in food processing caused an early shift toward a disease-associated oral microbiota in this population.
 Diet and the microbial aetiology of dental caries: new paradigms. Bradshaw DJ & Lynch RJ. International Dental Journal 2013
Many authors described caries as a transmissible infectious disease. However, more recent data have shifted these paradigms. Streptococcus mutans does not fulfil Koch’s postulates – presence of the organism leading to disease, and absence of the organism precluding disease. Furthermore, molecular microbiological methods have shown that, even with a sugar-rich diet, a much broader spectrum of acidogenic microbes is found in dental plaque. While simple sugars can be cariogenic, cooked starches are also now recognised to be a caries threat, especially because such starches, while not ‘sticky in the hand’, can be highly retentive in the mouth.
Central African rainforest environments show great plant and animal biodiversity, including above-ground edible plants and starch-rich plant underground storage organs (USOs), as well as many accessible prey animals. Ethnographic evidence has shown that foraging activities, mainly providing wild yam tubers (Dioscorea spp.), supply the bulk of the diet among [pygmy], who rarely spend time cultivating plant foods.
 Interview with a Kitavan, Stephan Guyenet, Whole Health Source, Dec 2010
 Remarks on THE INFLUENCE OF A CEREAL-FREE DIET RICH IN VITAMIN D AND CALCIUM ON DENTAL CARIES IN CHILDREN May Mellanby & C. Lee Pattison The British Medical Journal, 1932
 Improving the bioavailability of nutrients in plant foods at the household level. Gibson et al, The Procedings of the Nutrition Society, 2006
Increases in Fe, Zn and Ca absorption have been reported in adults fed dephytinized cereals compared with cereals containing their native phytate.
 Nutritional rickets: deficiency of vitamin D, calcium, or both? American Journal of Clinical Nutrition 2004
In sunny countries such as Nigeria, South Africa, and Bangladesh, such factors (vitamin D deficiency) do not apply. Studies indicated that the disease occurs among older toddlers and children and probably is attributable to low dietary calcium intakes, which are characteristic of cereal-based diets with limited variety and little access to dairy products.
 Baby dies of rickets from vegetarian mother, The Telegraph, Jan 2014
 Infants and children consuming atypical diets: Vegetarianism and macrobiotics Tanya Di Genova, Pediatr Child Health, 2007
…iron deficiency anemia has been shown in many studies to occur in vegetarian children and in a greater proportion of macrobiotic children… Calcium intake for vegan and macrobiotic children may be below current recommendations, and their diets may contain substances found in plant foods that may impair calcium absorption. Low calcium may result in rickets and reduced bone mineral content or osteoporosis, with important implications for future fracture risk.
 Meat consumption reduces the risk of nutritional rickets and osteomalacia. Dunnigan et al. The British Journal of Nutrition, 2005
The mechanism by which meat reduces rachitic and osteomalacic risk is uncertain and appears independent of revised estimates of meat vitamin D content. The meat content of the omnivore Western diet may explain its high degree of protection against nutritional rickets and osteomalacia from infancy to old age in the presence of endogenous vitamin D deficiency
 Chapter 5 – Isolated and modernized Eskimos, Nutrition and Physical Degeneration (book), Weston A. Price, 1939
The excellence of dentitions among the Eskimos has been a characteristic also of the skulls that have been excavated in various parts of Alaska… When these adult Eskimos exchange their foods for our modern foods… they often have very extensive tooth decay and suffer severely.
 Porotic Hyperostosis and Cribra Orbitalia Jess Beck, Bone Broke, 2014
It has long been acknowledged that the frequency of porotic hyperostosis increases regionally with the adoption of agriculture (Cohen & Armelagos 1984), and the ‘maize-dependency’ hypothesis suggests that a reliance on cereal grains, which are low in iron, as staple foods, led to the fluorescence of porotic hyperostosis that appeared subsequent to the increasing reliance on domesticated crops around the world. In addition to being poor sources of iron themselves, cereal grains like maize contain phytic acid, which has a deleterious effect on the ability of the intestine to absorb dietary iron (Holland & O’Brien 1997).