Cited by 621Oral microbiology and periodontitis researchPaleopathology and ancient diseasesForensic and Genetic Research

Sequencing ancient calcified dental plaque shows changes in oral microbiota with dietary shifts of the Neolithic and Industrial revolutions

Open access
Adler, Christina J, Dobney, Keith, Weyrich, Laura S, Kaidonis, John, Walker, Alan W, Haak, Wolfgang, Bradshaw, Corey J A, Townsend, Grant +4 more·2013·Nature Genetics

Abstract

The importance of commensal microbes for human health is increasingly recognized, yet the impacts of evolutionary changes in human diet and culture on commensal microbiota remain almost unknown. 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). Here, we show that calcified dental plaque (dental calculus) on ancient teeth preserves a detailed genetic record throughout this period. Data from 34 early European skeletons indicate that the transition from hunter-gatherer to farming shifted the oral microbial community to a disease-associated configuration. The composition of oral microbiota remained unexpectedly constant between Neolithic and medieval times, after which (the now ubiquitous) cariogenic bacteria became dominant, apparently during the Industrial Revolution. Modern oral microbiotic ecosystems are markedly less diverse than historic populations, which might be contributing to chronic oral (and other) disease in postindustrial lifestyles.

AI snapshot

Written from the paper’s full text.

TL;DR

Sequencing ancient dental calculus from 34 European skeletons shows that the oral microbiota shifted to a disease-associated configuration with Neolithic farming, remained relatively constant through Medieval times, and became less diverse and more cariogenic after the Industrial Revolution. Modern oral microbiota are markedly less diverse than historic populations.

Key findings

  • Ancient calculus preserved oral microbial signatures: it was dominated by Firmicutes (33% for the V3 region), comparable to the Human Oral Microbiome Database (37%) and modern oral samples (average 50%), and distinct from extraction blanks (6% Firmicutes, p = 0.003), environmental samples (1.6%, p < 0.001), and within ancient teeth (8%, p < 0.001). Ancient calculus also contained all 15 phyla commonly found in the modern human oral cavity, with high Actinobacteria (19%) as observed in modern calculus deposits (7%).
  • The transition from hunter-gatherer to farming shifted the oral microbial community to a disease-associated configuration: hunter-gatherers displayed fewer caries- and periodontal disease-associated taxa, while farming populations had more periodontal disease-associated taxa, including P. gingivalis, Tannerella, and Treponema. Composition remained notably consistent from the Neolithic through the Medieval period.
  • Modern oral environments were much less biodiverse and dominated by potentially cariogenic bacteria; the frequency of S. mutans was significantly higher in modern samples than pre-industrial agricultural samples, and modern Europeans had lower oral microbial diversity than Mesolithic or pre-Industrial Neolithic groups (p < 0.001). Random forest analysis identified Clostridiales (importance score = 0.014 ± 0.002) and Ruminococcaceae (0.0035 ± 0.0009) as predictive of hunter-gatherer versus early agriculturist communities (ratio baseline error to observed error = 3.5), and Veillonellaceae (0.021 ± 0.004), Lachnospiraceae (0.019 ± 0.007), and Actinomycetales (0.0013 ± 0.0005) as distinguishing modern from farming groups (ratio = 4.0).
  • Periodontal disease-associated bacteria were relatively stable since the introduction of farming, which the authors argue indicates that although periodontal disease might contribute to pathogenesis, it is probably not a factor in the rising incidence of systemic diseases.

Methods

  • The study analyzed supra- and subgingival calculus from 34 prehistoric European skeletons (11 males, 11 females, 12 unknown sex; age at death from <20 to >60 years) dating from the Mesolithic to Medieval periods, compared with modern calculus (n = 6), modern plaque (n = 13), ancient tooth samples (n = 6), and extraction blanks.
  • DNA was extracted from 0.05–0.2 g of sterilized, powdered ancient calculus; PCR amplicon libraries targeted three hypervariable regions of the 16S rRNA gene (V1, V3, V6) with barcoded primers, plus specific primers for Streptococcus mutans (GtfB gene) and Porphyromonas gingivalis (16S rRNA gene). Sequencing used 454 GS FLX Titanium, and analysis used QIIME 1.5.0, quality filtering, denoising, UCLUST OTU picking at 95% likeness, RDP classification, and random forest/diversity analyses.
  • Of 998,575 sequences generated, about 50% were discarded after quality filtering and denoising, leaving 451,241 sequences.

Limitations

  • Stated in the paper: independent extractions were not possible because of the small size of samples, and commonly only one calculus deposit per individual was available for DNA analysis. The authors also attempted unsuccessfully to amplify human mtDNA from the ancient dental calculus samples.
  • Evident from the text: the 16S rRNA amplicons were short (60–210 bp) and OTUs were clustered at 95% rather than the more common 97%, which may limit taxonomic resolution for closely related taxa.
  • Evident from the text: the temporal comparisons rest on 34 skeletons spanning a broad period, and the paper does not report per-period sample sizes in the provided text, so the robustness of period-specific contrasts is not fully clear from the main text alone.

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Integrity signals

Registry

Crossref · 10.1038/ng.2536

Cites

88 of 88 references verified0 citation errors · 0 not checkable

Statistics

Nothing to recompute.

Claims the paper makes

0 of 45 cited sources checked · 0 supported · 0 flagged

  • Findingown data

    Periodontal disease-associated taxa were found across a range of ages, including the youngest individual (3-4 years old, ID 8247).

    “While there is also a strong association between periodontal disease and individual age at death42, we found periodontal disease-associated taxa across a range of ages, including the youngest individual (3-4 years old, ID 8247).”
    Quote in the paperNot a substantial claim
  • Findingown data

    After the transition to agriculture in the early Neolithic, there was notable consistency in bacterial composition through the Medieval period (~400 years BP).

    “After the transition to agriculture in the early Neolithic there was a notable consistency in the composition of bacteria through the Medieval period (~ 400 years BP) (Figure 3), in parallel with the broad similarity of food-processing technologies during these times9.”
    Quote in the paperSubstantial claim
  • Findingown data

    The taxa distinguishing modern oral environments from farming groups include decay-associated Veillonellaceae, Lachnospiraceae, and Actinomycetales.

    “These taxa include decay-associated Veillonellaceae (importance score = 0.021 ± 0.004), in addition to Lachnospiraceae (importance score= 0.019 ± 0.007) and Actinomycetales (importance score = 0.0013 ± 0.0005).”
    Quote in the paperSubstantial claim
  • Findingown data

    Earlier hunter-gatherer groups displayed fewer caries- and periodontal disease-associated taxa than farming groups.

    “The composition of oral microbiota underwent a distinct shift with the introduction of farming in the early Neolithic (Figures 2c and d), with the earlier hunter-gatherer groups displaying fewer caries- and periodontal disease-associated taxa (Figure 3).”
    Quote in the paperSubstantial claim
  • Findingown data

    Random forest analysis revealed that only a limited number of taxa distinguished modern oral environments from farming groups in the Medieval and Neolithic periods (ratio baseline error to observed error = 4.0).

    “RF analysis revealed that only a limited number of taxa distinguished modern oral environments from farming groups in the Medieval and Neolithic periods (ratio baseline error to observed error = 4.0 , Supplementary Table 9).”
    Quote in the paperSubstantial claim
  • May combine two claims. 15
  • The quote only partly states this claim. 1
  • Classified as probably not a substantial claim. 8
  • May combine two claims.

    Findingown data

    The Firmicutes percentage in ancient calculus is significantly higher than in extraction blanks (6%, p = 0.003), environmental samples (1.6%, p < 0.001), and ancient teeth (8%, p < 0.001).

    “Again, this was clearly distinguishable from the bacterial sequences obtained from extraction blanks (6% Firmicutes, p = 0.003), environmental samples (1.6% Firmicutes, p < 0.001) and within the ancient teeth (8% Firmicutes, p < 0.001), which were all dominated by Proteobacteria (73% p = 0.2, 56% p < 0.001 and 31% p = 0.005, respectively).”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Findingown data

    The bacterial composition of ancient dental calculus is similar to modern oral samples and the Human Oral Microbiome Database, but markedly distinct from laboratory reagents, environmental samples, and ancient teeth.

    “At the phylum level, the bacterial composition of ancient calculus was similar to modern oral samples and sequences from the Human Oral Microbiome Database (HOMD)30, but markedly distinct from laboratory reagents (extraction blanks), environmental samples (soils, sediments and water), and within the ancient teeth themselves (Figure 1, Supplementary Fig. 2 and Supplementary Note).”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Findingown data

    Ancient dental calculus was dominated by Firmicutes (33% for the V3 region), comparable to percentages in the Human Oral Microbiome Database (37%) and modern oral samples (average 50%).

    “The archaeological calculus was dominated by Firmicutes (33% for the V3 region, which was the most phylogenetically informative fragment, see Supplementary Note), which is comparable to percentages found in both the HOMD (37%), and modern oral samples (average 50%)1,2,21,31.”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Findingown data

    Modern oral samples have fewer bacteria associated with good health (Ruminococcaceae), periodontal disease-associated taxa similar to early agriculturists, and a markedly higher abundance of pathogens such as Streptococcus mutans.

    “Overall, it is clear that modern Europeans have much lower oral microbial diversity than either Mesolithic or pre-Industrial Neolithic groups (p < 0.001, Supplementary Table 7), including fewer bacteria associated with good health (Ruminococcaceae), periodontal disease-associated taxa (e.g., Porphyromonas gingivalis, Tannerella and Treponema) similar to early agriculturists, and a markedly higher”
    Quote in the paperSubstantial claim
  • The quote only partly states this claim.

    Findingown data

    Similar patterns of similarity to modern oral samples were observed for V1 and V6 sequences.

    “Similar patterns were observed for sequences from V1 and V6 (Supplementary Fig. 5, Supplementary Note).”
    Quote in the paperNot a substantial claim
  • May combine two claims.

    Findingown data

    Today's oral environment is much less biodiverse and dominated by potentially cariogenic bacteria such as S. mutans.

    “In contrast, today’s oral environment is much less biodiverse and dominated by potentially cariogenic bacteria (Figure 3a and b, e.g., S. mutans, Supplementary Figs. 7-9 and Supplementary Table 7).”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Findingown data

    Ancient dental calculus samples contained all 15 phyla commonly found in the modern human oral cavity, with high percentages of Actinobacteria (19%) as observed in modern calculus deposits (7%).

    “In addition to Firmicutes, the ancient dental calculus samples contained all 15 phyla commonly found in the modern human oral cavity30, with high percentages of Actinobacteria (19%) as is observed in modern calculus deposits (7%).”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Premisecitation

    The Industrial Revolution saw the production of refined grain and concentrated sugar, generating mono- and disaccharides that are the main substrates for microbial fermentation that lowers plaque pH and causes enamel demineralization.

    “The Industrial Revolution saw the production of refined grain and concentrated sugar from processed sugar beet and cane9, generating mono- and disaccharides, which are the main substrates for microbial fermentation that lowers plaque pH and cause enamel demineralization26.”
    Quote in the paperSubstantial claim0 of 2 sources checked
    • cites [9] Cordain, L. et al. Origins and evolution of the Western diet: health implications for the 21st century. Am. J. Clin. Nutr. 81, 341–354 (2005). source

      Not checked in the free run.

    • cites [26] Marsh, P.D. Microbiology of dental plaque biofilms and their role in oral health and caries. Dent. Clin. North Am. 54, 441–454 (2010). source

      Not checked in the free run.

  • May combine two claims.

    Interpretationcitation

    The shift in oral microbiota with farming is consistent with skeletal evidence of marked increases in periodontal disease following the transition to an agricultural diet, suggesting a major impact on the human oral ecosystem around this time.

    “This is consistent with skeletal evidence showing marked increases in periodontal disease41 following the transition to an agricultural diet, suggesting a major impact on the human oral ecosystem around this time.”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [41] Kerr, N.W. Prevalence and natural history of periodontal disease in prehistoric Scots (pre-900 AD). J. Periodontal Res. 33, 131–137 (1998). source

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    Oral bacteria are associated with many systemic diseases including arthritis, cardiovascular disease, and diabetes.

    “Notably, oral bacteria are also associated with many systemic diseases including arthritis28, cardiovascular disease3 and diabetes4, in addition to diseases of the oral cavity1,2.”
    Quote in the paperNot a substantial claim0 of 3 sources checked
    • cites [28] Mercado, F.B., Marshall, R.I., Klestov, A.C. & Bartold, P.M. Relationship between rheumatoid arthritis and periodontitis. J. Periodontol. 72, 779–787 (2001). source

      Not checked in the free run.

    • cites [3] Davé, S. & Van Dyke, T. The link between periodontal disease and cardiovascular disease is probably inflammation. Oral Dis. 14, 95–101 (2008). source

      Not checked in the free run.

    • cites [4] Grossi, S.G. & Genco, R.J. Periodontal disease and diabetes mellitus: a two-way relationship. Ann. Periodontol. 3, 51–61 (1998). source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    Dental caries and periodontal disease were rare in pre-Neolithic hunter-gatherer societies and early hominins.

    “These oral diseases include dental caries (tooth decay)1 and periodontal disease (an infection causing damage to the supporting connective tissues of the tooth and resorption of bone)21, both of which were rare in pre-Neolithic hunter-gatherer societies20 and early hominins22.”
    Quote in the paperSubstantial claim0 of 2 sources checked
    • cites [20] Aufderheide, A.C., Rodriguez-Martin, C. & Langsjoen, O. The Cambridge Encyclopedia of Human Paleopathology (Cambridge University Press, Cambridge, 1998).

      Not checked in the free run.

    • cites [22] Grine, F.E., Gwinnett, A.J. & Oaks, J.H. Early hominid dental pathology: interproximal caries in 1.5 million-year-old Paranthropus robustus from Swartkrans. Arch. Oral Biol. 35, 381–386 (1990). source

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Premisecitation

    Commensal microbiota comprise the majority of cells in the body and play a key role in human health.

    “Commensal microbiota comprise the majority of cells in the body and play a key role in human health1-5,10.”
    Quote in the paperNot a substantial claim0 of 6 sources checked
    • cites [1] Aas, J.A. et al. Bacteria of dental caries in primary and permanent teeth in children and young adults. J. Clin. Microbiol. 46, 1407–1417 (2008). source

      Not checked in the free run.

    • cites [2] Aas, J.A., Paster, B.J., Stokes, L.N., Olsen, I. & Dewhirst, F.E. Defining the normal bacterial flora of the oral cavity. J. Clin. Microbiol. 43, 5721–5732 (2005). source

      Not checked in the free run.

    • cites [3] Davé, S. & Van Dyke, T. The link between periodontal disease and cardiovascular disease is probably inflammation. Oral Dis. 14, 95–101 (2008). source

      Not checked in the free run.

    • cites [4] Grossi, S.G. & Genco, R.J. Periodontal disease and diabetes mellitus: a two-way relationship. Ann. Periodontol. 3, 51–61 (1998). source

      Not checked in the free run.

    • cites [5] Human Microbiome Project Consortium. Structure, function and diversity of the healthy human microbiome. Nature 486, 207–214 (2012). source

      Not checked in the free run.

    • cites [10] Savage, D.C. Microbial ecology of the gastrointestinal tract. Annu. Rev. Microbiol. 31, 107–133 (1977). source

      Not checked in the free run.

  • Classified as probably not a substantial claim.

    Premisecitation

    The frequency of systemic diseases has risen over the last few decades.

    “However, whilst the frequency of these systemic diseases has risen over the last few decades25, our data show that the abundance of periodontal disease-associated bacteria has been relatively stable since the introduction of farming (e.g., Figure 3, P. gingivalis).”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [25] Hujoel, P. Dietary carbohydrates and dental-systemic diseases. J. Dent. Res. 88, 490–502 (2009). source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    Bacteria in calculus become locked in a crystalline matrix similar to bone, with deposits occurring both above and below the gum.

    “Bacteria in calculus become locked in a crystalline matrix similar to bone16 (Supplementary Figure 1), with deposits occurring both above and below the gum or gingiva (supra- and subgingivally)17.”
    Quote in the paperSubstantial claim0 of 2 sources checked
    • cites [16] Jin, Y. & Yip, H.K. Supragingival calculus: formation and control. Crit. Rev. Oral Biol. Med. 13, 426–441 (2002). source

      Not checked in the free run.

    • cites [17] Lieverse, A.R. Diet and the aetiology of dental calculus. Int. J. Osteoarchaeol. 9, 219–232 (1999). source

      Not checked in the free run.

  • May combine two claims.

    Interpretationown data

    Major changes in carbohydrate intake in human history appear to have impacted the ecosystem of the mouth, opening up pathological niches for periodontal disease in the early Neolithic and caries in the recent past.

    “Major changes in carbohydrate intake in human history appear to have impacted the ecosystem of the mouth, opening up pathological niches for periodontal disease in the early Neolithic and caries in the recent past.”
    Quote in the paperSubstantial claim
  • Classified as probably not a substantial claim.

    Premisecitation

    Dental calculus develops when dental plaque becomes mineralised with calcium phosphate.

    “Dental calculus develops when dental plaque, an extremely dense bacterial biofilm15, becomes mineralised with calcium phosphate16.”
    Quote in the paperSubstantial claim0 of 2 sources checked
    • cites [15] Socransky, S.S. & Haffajee, A.D. Dental biofilms: difficult therapeutic targets. Periodontol. 2000 28, 12–55 (2002). source

      Not checked in the free run.

    • cites [16] Jin, Y. & Yip, H.K. Supragingival calculus: formation and control. Crit. Rev. Oral Biol. Med. 13, 426–441 (2002). source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    Oral bacteria are transferred vertically from primary caregiver(s) in early childhood and horizontally between family members later in life.

    “In addition, oral bacteria are transferred vertically from the primary caregiver(s) in early childhood18 and horizontally between family members later in life18,19, making archaeological dental calculus a potentially unique means of tracing population structure, movement and admixture between ancient cultures, as well as the spread of diseases.”
    Quote in the paperSubstantial claim0 of 2 sources checked
    • cites [18] Asikainen, S., Chen, C. & Slots, J. Likelihood of transmitting Actinobacillus actinomycetemcomitans and Porphyromonas gingivalis in families with periodontitis. Oral Microbiol. Immunol. 11, 387–394 (1996). source

      Not checked in the free run.

    • cites [19] Van Steenbergen, T.J., Menard, C., Tijhof, C.J., Mouton, C. & De Graaff, J. Comparison of three molecular typing methods in studies of transmission of Porphyromonas gingivalis. J. Med. Microbiol. 39, 416–421 (1993). source

      Not checked in the free run.

  • Classified as probably not a substantial claim. May combine two claims.

    Premisecitation

    Caries and periodontal disease are polymicrobial, plaque-mediated infections thought to result from perturbation of a healthy, ecologically balanced oral biofilm that can occur from dietary changes such as increased consumption of fermentable carbohydrates.

    “Caries and periodontal disease are both polymicrobial, plaque-mediated infections, thought to result from perturbation of a healthy, ecologically balanced oral biofilm23,24 that can occur from dietary changes, such as the increased consumption of fermentable carbohydrates25,26.”
    Quote in the paperSubstantial claim0 of 4 sources checked
    • cites [23] Marsh, P.D. Sugar, fluoride, pH and microbial homeostasis in dental plaque. Proc. Finn. Dent. Soc. 87, 515–525 (1991).

      Not checked in the free run.

    • cites [24] Marsh, P.D. Are dental diseases examples of ecological catastrophes? Microbiology 149, 279–294 (2003). source

      Not checked in the free run.

    • cites [25] Hujoel, P. Dietary carbohydrates and dental-systemic diseases. J. Dent. Res. 88, 490–502 (2009). source

      Not checked in the free run.

    • cites [26] Marsh, P.D. Microbiology of dental plaque biofilms and their role in oral health and caries. Dent. Clin. North Am. 54, 441–454 (2010). source

      Not checked in the free run.

  • Classified as probably not a substantial claim.

    Premisecitation

    The adoption of carbohydrate-rich Neolithic farming diets began approximately 10,000 years BP.

    “Two of the greatest dietary shifts in human evolution involved the adoption of carbohydrate-rich Neolithic (farming) diets6,7 (beginning ~10,000 years BP6,8), and the more recent advent of industrially processed flour and sugar (~1850)9.”
    Quote in the paperSubstantial claim0 of 3 sources checked
    • cites [6] Braidwood, R.J., Howe, B. & Reed, C.A. The Iranian Prehistoric Project: new problems arise as more is learned of the first attempts at food production and settled village life. Science 133, 2008–2010 (1961). source

      Not checked in the free run.

    • cites [7] Oelzea, V.M. et al. Early Neolithic diet and animal husbandry: stable isotope evidence from three Linearbandkeramik (LBK) sites in Central Germany. J. Archaeol. Sci. 38, 270–279 (2011). source

      Not checked in the free run.

    • cites [8] Childe, V.G. The Dawn of European Civilisation (Kegan Paul, London, 1925).

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    The impact of farming on the oral ecosystem is thought to be caused by increased amounts of soft carbohydrate foods compared with hunter-gatherer diets.

    “This is thought to be caused by increased amounts of soft carbohydrate foods compared with hunter-gatherer diets26.”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [26] Marsh, P.D. Microbiology of dental plaque biofilms and their role in oral health and caries. Dent. Clin. North Am. 54, 441–454 (2010). source

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Premisecitation

    The Industrial Revolution began some 200 years ago and represents the largest change in food production and processing technology since the shift to farming.

    “This change is most likely associated with the onset of the Industrial Revolution which began some 200 years ago and represents the largest change in food production and processing technology since the shift to farming9.”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [9] Cordain, L. et al. Origins and evolution of the Western diet: health implications for the 21st century. Am. J. Clin. Nutr. 81, 341–354 (2005). source

      Not checked in the free run.

21 of 21
  • The paper relies on this without support.

    Detailed genetic records from commensal bacteria have not yet been recovered from the archaeological record.

    “However, their evolution remains poorly understood, and detailed genetic records from commensal bacteria have yet to be recovered from the archaeological record.”
  • The paper relies on this without support.

    The impacts of evolutionary changes in human diet and culture on commensal microbiota remain almost unknown.

    “yet the impacts of evolutionary changes in human diet and culture on commensal microbiota remain almost unknown.”
2 of 2

Claims other papers make about this one

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Cites

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Research works printed but not linked: 2

  1. Lilley, J., Stroud, G. & Brothwell, D. The Jewish burial ground at Jewbury. in The Archaeology of York Vol. 12 (eds. Addyman, P.V. & Kinsler, V.A.) 291–578 (Council for British Archaeology, York, UK, 1994).
  2. Vandermeersch, B. et al. Middle Palaeolithic dental bacteria from Kebara, Israel. C.R. Acad. Sci. Paris 319, 727–731 (1994).

Cited by

Sorted by citations

Authors
Adler, C. J., Dobney, K., Weyrich, L. S., Kaidonis, J., Walker, A. W., Haak, W., Bradshaw, C. J. A., Townsend, G., Sołtysiak, A., Alt, K. W., Parkhill, J., & Cooper, A.
Affiliations
  • The University of Adelaide (AU)
  • University of Aberdeen (GB)
  • Wellcome Sanger Institute (GB)
  • South Australian Research and Development Institute (AU)
  • University of Warsaw (PL)
  • Johannes Gutenberg University Mainz (DE)
Corresponding author
Cooper, Alan
Venue
Nature Genetics
Published
2013-02-17
Volume
45
Issue
4
Pages
450-455
ISSN
  • 1061-4036 (ISSN-L)
  • 1546-1718
OpenAlex
W2024189200
Cited by
621
References
88
Citations by year
2026: 26 · 2025: 28 · 2024: 38 · 2023: 40 · 2022: 49 · 2021: 63 · 2020: 56 · 2019: 59 · 2018: 63 · 2017: 49 · 2016: 52 · 2015: 37 · 2014: 44 · 2013: 17
FWCI
60.76
Type
journal article
Language
en
Open access
Locations
  • Nature Genetics (publishedVersion)
  • PubMed (publishedVersion)
  • PubMed Central (acceptedVersion)
  • Europe PMC (PubMed Central) (acceptedVersion)
  • Aberdeen University Research Archive (Aberdeen University) (submittedVersion)
  • Adelaide Research & Scholarship (AR&S) (University of Adelaide) (submittedVersion)
  • MPG.PuRe (Max Planck Society) (submittedVersion)
Funders
Wellcome Trust (WT092799/Z/10/Z, 076964, WT076964, WT 098051, WT092799MA)
Topics
  • Health Sciences › Dentistry › Periodontics › Oral microbiology and periodontitis research
  • Social Sciences › Arts and Humanities › Archeology › Paleopathology and ancient diseases
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Forensic and Genetic Research
Keywords
oral microbiota, dental calculus, ancient DNA, Neolithic transition, Industrial Revolution, hunter-gatherers, cariogenic bacteria, dietary change, microbial diversity, sugar consumption, oral diseases
MeSH terms
Archaeology, Dental Plaque, Diet, Biological Evolution, Humans, Industry, Mouth Mucosa, Metagenome, High-Throughput Nucleotide Sequencing

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