Detection and Molecular Characterization of 9000-Year-Old Mycobacterium tuberculosis from a Neolithic Settlement in the Eastern Mediterranean
Open accessAbstract
BACKGROUND: Mycobacterium tuberculosis is the principal etiologic agent of human tuberculosis. It has no environmental reservoir and is believed to have co-evolved with its host over millennia. This is supported by skeletal evidence of the disease in early humans, and inferred from M. tuberculosis genomic analysis. Direct examination of ancient human remains for M. tuberculosis biomarkers should aid our understanding of the nature of prehistoric tuberculosis and the host/pathogen relationship. METHODOLOGY/PRINCIPAL FINDINGS: We used conventional PCR to examine bone samples with typical tuberculosis lesions from a woman and infant, who were buried together in the now submerged site of Atlit-Yam in the Eastern Mediterranean, dating from 9,250-8,160 years ago. Rigorous precautions were taken to prevent contamination, and independent centers were used to confirm authenticity of findings. DNA from five M tuberculosis genetic loci was detected and had characteristics consistent with extant genetic lineages. High performance liquid chromatography was used as an independent method of verification and it directly detected mycolic acid lipid biomarkers, specific for the M. tuberculosis complex. CONCLUSIONS/SIGNIFICANCE: Human tuberculosis was confirmed by morphological and molecular methods in a population living in one of the first villages with evidence of agriculture and animal domestication. The widespread use of animals was not a source of infection but may have supported a denser human population that facilitated transmission of the tubercle bacillus. The similarity of the M. tuberculosis genetic signature with those of today gives support to the theory of a long-term co-existence of host and pathogen.
Verifying this paper
8 of 9 steps done · this page updates itself — you can leave and come back
- Registry recordVerified
- Full textRead the full text
- Reference list51 references found
- Reference checkChecking each cited work — 51 of 51
- StatisticsNeeds the full text
- ClaimsNeeds the full text
- Cited sourcesNeeds claims to check
- Self-checkNeeds the full text
- VerificationFindings verified
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
The identification of M. tuberculosis from an individual approximately 2,000 years ago is consistent with our current understanding of Mycobacterium infection and transmission between humans and in humans and domesticated animals.
“The identification of M. tuberculosis from an individual approximately 2,000 years ago is consistent with our current understanding of Mycobacterium infection and transmission between humans and in humans and domesticated animals [40].”
From Molecular Exploration of the First-Century Tomb of the Shroud in Akeldama, Jerusalem (2009) · cites this paper as [40]
The Introduction reports M. tuberculosis in human remains, and the Discussion links its transmission to denser human populations. But the studied remains date to 9,250–8,160 years ago, not approximately 2,000 years ago. The paper also says domesticated animals were not the source of infection in this population; it does not establish transmission between humans and domesticated animals. (LLM, conf=0.88)
Experimental — accuracy not yet measured
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Kamerbeek, J., Schouls, L. M., Kolk, A. H. J., van Agterveld, M., van Soolingen, D., Kuijper, S., Bunschoten, A., Molhuizen, H. O. F., Shaw, R. J., Goyal, M., et al. (1997) · Journal of Clinical Microbiology · doi:10.1128/jcm.35.4.907-914.1997 · Cited by 2,871 · see citing works
Identification of Pathological Conditions in Human Skeletal Remains
Ortner, D. J. (2003) · Elsevier eBooks · doi:10.1016/b978-0-12-528628-2.x5037-6 · Cited by 2,526 · see citing works
A new evolutionary scenario for the Mycobacterium tuberculosis complex
Brosch, R., Gordon, S. V., Marmiesse, M., Brodin, P. M., Buchrieser, C., Eiglmeier, K., Garnier, T., Gutierrez, C., Hewinson, R. G., Kremer, K., et al. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.052548299 · Cited by 1,645 · see citing works
Paleopathology at the Origins of Agriculture.
Dennell, R., Cohen, M. N., & Armelagos, G. J. (1986) · Man · doi:10.2307/2803166 · Cited by 1,336 · see citing works
Identification of pathological conditions in human skeletal remains
Ortner, D. J., & Putschar, W. G. J. (1985) · Smithsonian contributions to anthropology · doi:10.5479/si.00810223.28.1 · Cited by 1,059 · see citing works
Sreevatsan, S., Pan, X., Stockbauer, K. E., Connell, N. D., Kreiswirth, B. N., Whittam, T. S., & Musser, J. M. (1997) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.94.18.9869 · Cited by 1,035 · see citing works
The epidemiology of Mycobacterium bovis infections in animals and man: A review
O'Reilly, L. M., & Daborn, C. J. (1995) · Tubercle and Lung Disease · doi:10.1016/0962-8479(95)90591-x · Cited by 835 · see citing works
Daniel, T. M. (2006) · Respiratory Medicine · doi:10.1016/j.rmed.2006.08.006 · Cited by 765 · see citing works
Eisenach, K. D., Donald Cave, M., Bates, J. H., & Crawford, J. T. (1990) · Journal of Infectious Diseases · doi:10.1093/infdis/161.5.977 · Cited by 748 · see citing works
Social and environmental risk factors in the emergence of infectious diseases
Weiss, R. A., & McMichael, A. J. (2004) · Nature Medicine · doi:10.1038/nm1150 · Cited by 714 · see citing works
Ancient Origin and Gene Mosaicism of the Progenitor of Mycobacterium tuberculosis
Gutierrez, M. C., Brisse, S., Brosch, R., Fabre, M., Omaïs, B., Marmiesse, M., Supply, P., & Vincent, V. (2005) · PLoS Pathogens · doi:10.1371/journal.ppat.0010005 · Cited by 646 · see citing works
Origin, Spread and Demography of the Mycobacterium tuberculosis Complex
Wirth, T., Hildebrand, F., Allix‐Béguec, C., Wölbeling, F., Kubica, T., Kremer, K., van Soolingen, D., Rüsch–Gerdes, S., Locht, C., Brisse, S., et al. (2008) · PLoS Pathogens · doi:10.1371/journal.ppat.1000160 · Cited by 513 · see citing works
Environmental and social influences on emerging infectious diseases: past, present and future
McMichael, A. J. (2004) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2004.1480 · Cited by 418 · see citing works
Stable association between strains of Mycobacterium tuberculosis and their human host populations
Hirsh, A. E., Tsolaki, A. G., DeRiemer, K., Feldman, M. W., & Small, P. M. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0305627101 · Cited by 401 · see citing works
Characterization ofMycobacterium tuberculosisComplex DNAs from Egyptian Mummies by Spoligotyping
Zink, A., Sola, C., Reischl, U., Grabner, W., Rastogi, N., Wolf, H. J., & Nerlich, M. L. (2003) · Journal of Clinical Microbiology · doi:10.1128/jcm.41.1.359-367.2003 · Cited by 297 · see citing works
Mycobacterium tuberculosisComplex DNA from an Extinct Bison Dated 17,000 Years before the Present
Rothschild, B. M., Martin, L. D., Lev, G., Bercovier, H., Bar‐Gal, G. K., Greenblatt, C. L., Donoghue, H. D., Spigelman, M., & Brittain, D. (2001) · Clinical Infectious Diseases · doi:10.1086/321886 · Cited by 292 · see citing works
Self-citationThe Methyl-Branched Fortifications of Mycobacterium tuberculosis
Minnikin, D. E., Kremer, L., Dover, L. G., & Besra, G. S. (2002) · Chemistry & Biology · doi:10.1016/s1074-5521(02)00142-4 · Cited by 268 · see citing works
Self-citationPEARCE‐DUVET, J. M. C. (2006) · Biological reviews/Biological reviews of the Cambridge Philosophical Society · doi:10.1017/s1464793106007020 · Cited by 268 · see citing works
Parsons, L. M., Brosch, R., Cole, S. T., Somoskövi, Á., Loder, A., Bretzel, G., van Soolingen, D., Hale, Y. M., & Salfinger, M. (2002) · Journal of Clinical Microbiology · doi:10.1128/jcm.40.7.2339-2345.2002 · Cited by 243 · see citing works
Mensforth, R. P., Lovejoy, C. O., Lallo, J. W., & Armelagos, G. J. (1978) · Medical Anthropology · doi:10.1080/01459740.1978.9986939 · Cited by 241 · see citing works
Genomic Deletions Suggest a Phylogeny for theMycobacterium tuberculosisComplex
Mostowy, S., Cousins, D., Brinkman, J., Aranaz, A., & Behr, M. A. (2002) · The Journal of Infectious Diseases · doi:10.1086/341068 · Cited by 240 · see citing works
Tuberculosis: from prehistory to Robert Koch, as revealed by ancient DNA
Donoghue, H. D., Spigelman, M., Greenblatt, C. L., Lev-Maor, G., Bar‐Gal, G. K., Matheson, C., Vernon, K. K., Nerlich, M. L., & Zink, A. (2004) · The Lancet Infectious Diseases · doi:10.1016/s1473-3099(04)01133-8 · Cited by 214 · see citing works
Self-citationFirst Homo erectus from Turkey and implications for migrations into temperate Eurasia
Kappelman, J. W., Alçiçek, M. C., Kazancı, N., Schultz, M., Özkul, M., & Şen, Ş. (2007) · American Journal of Physical Anthropology · doi:10.1002/ajpa.20739 · Cited by 210 · see citing works
Huard, R. C., Fabre, M., de Haas, P., Lazzarini, L. C. O., van Soolingen, D., Cousins, D., & Ho, J. L. (2006) · Journal of Bacteriology · doi:10.1128/jb.01783-05 · Cited by 194 · see citing works
Molecular analysis of skeletal tuberculosis in an ancient Egyptian population
Zink, A., Haas, C. J., Reischl, U., Szeimies, U., & Nerlich, M. L. (2001) · Journal of Medical Microbiology · doi:10.1099/0022-1317-50-4-355 · Cited by 188 · see citing works
Paleopathological Diagnosis and Interpretation: Bone Diseases in Ancient Human Populations
Steinbock, R. T. (1976) · Cited by 188 · see citing works
Palaeomicrobiology: current issues and perspectives
Drancourt, M., & Raoult, D. (2004) · Nature Reviews Microbiology · doi:10.1038/nrmicro1063 · Cited by 185 · see citing works
Atlit-Yam: A Prehistoric Site on the Sea Floor off the Israeli Coast
Galili, E., Weinstein‐Evron, M., Hershkovitz, I., Gopher, A., Kislev, M., Lernau, O., Horwitz, L. K., & Lernau, H. (1993) · Journal of Field Archaeology · doi:10.1179/jfa.1993.20.2.133 · Cited by 178 · see citing works
Self-citationPediatric tuberculosis: time for a new approach
Starke, J. R. (2003) · Tuberculosis · doi:10.1016/s1472-9792(02)00088-4 · Cited by 153 · see citing works
Global epidemiology of paediatric tuberculosis
Walls, T., & Shingadia, D. V. (2003) · Journal of Infection · doi:10.1016/s0163-4453(03)00121-x · Cited by 143 · see citing works
Hershkovitz, I., Greenwald, C. M., Latimer, B., Jellema, L. M., Wish‐Baratz, S., Eshed, V., Dutour, O., & Rothschild, B. M. (2002) · American Journal of Physical Anthropology · doi:10.1002/ajpa.10077 · Cited by 131 · see citing works
Self-citationTuberculosis and leprosy in antiquity: an interpretation
Manchester, K. (1984) · Medical History · doi:10.1017/s0025727300035705 · Cited by 129 · see citing works
Mycobacterium tuberculosis complex DNA in calcified pleura from remains 1400 years old
Donoghue, H. D., Spigelman, M., Zias, J., Gernaey, A. M., & Minnikin, D. E. (1998) · Letters in Applied Microbiology · doi:10.1046/j.1472-765x.1998.t01-8-00449.x · Cited by 108 · see citing works
Self-citationFormicola, V., Milanesi, Q., & Scarsini, C. (1987) · American Journal of Physical Anthropology · doi:10.1002/ajpa.1330720102 · Cited by 106 · see citing works
DNA from Identified in Mediaeval Human Skeletal Remains Using Polymerase Chain Reaction
Taylor, M. G., Crossey, M. M. E., Saldanha, J., & Waldron, T. (1996) · Journal of Archaeological Science · doi:10.1006/jasc.1996.0073 · Cited by 98 · see citing works
Hughes, A. L., Friedman, R., & Murray, M. B. (2002) · Emerging infectious diseases · doi:10.3201/eid0811.020064 · Cited by 89 · see citing works
Mycolic acids and ancient DNA confirm an osteological diagnosis of tuberculosis
Gernaey, A. M., Minnikin, D. E., Copley, M. S., DIXON, R. A., Middleton, J. C., & Roberts, C. A. (2001) · Tuberculosis · doi:10.1054/tube.2001.0295 · Cited by 84 · see citing works
Self-citationMycobacterium bovis in England and Wales: past, present and future.
Hardie, R., & Watson, J. M. (1992) · PubMed Central · Cited by 81 · see citing works
Genotypic Analysis of the Earliest Known Prehistoric Case of Tuberculosis in Britain
Taylor, G. M., Young, D. B., & Mays, S. (2005) · Journal of Clinical Microbiology · doi:10.1128/jcm.43.5.2236-2240.2005 · Cited by 78 · see citing works
New Evidence of Tuberculous Spondylitis from Neolithic Liguria (Italy)
Canci, A., Minozzi, S., & Tarli, S. M. B. (1996) · International Journal of Osteoarchaeology · doi:10.1002/(sici)1099-1212(199612)6:5 · Cited by 68 · see citing works
Galili, E., Rosen, B., Gopher, A., & Horwitz, L. K. (2003) · Journal of Mediterranean Archaeology · doi:10.1558/jmea.v15i2.167 · Cited by 63 · see citing works
Self-citationRecognition of hypertrophic osteoarthropathy in skeletal remains.
Rothschild, B. M., & Rothschild, C. (1998) · PubMed · Cited by 60 · see citing works
The Evolution of Mycobacterial Disease in Human Populations: A Reevaluation [and Comments and Reply]
Clark, G. A., Kelley, M. A., Grange, J. M., Hill, M. C., Katzenberg, M. A., Klepinger, L. L., Lovell, N. C., McGrath, J. W., Micozzi, M. S., & Steinbock, R. T. (1987) · Current Anthropology · doi:10.1086/203490 · Cited by 48 · see citing works
Mays, S., & Taylor, G. M. (2002) · Journal of Archaeological Science · doi:10.1006/jasc.2001.0769 · Cited by 48 · see citing works
Emerging pathogens. Archaeology, ecology and evolution of infectious disease
Cox, F. E. G. (2003) · Transactions of the Royal Society of Tropical Medicine and Hygiene · doi:10.1016/s0035-9203(03)90103-9 · Cited by 43 · see citing works
8000 year-old human remains on the sea floor near Atlit, Israel
Hershkovitz, I., & Galili, E. (1990) · Human Evolution · doi:10.1007/bf02437249 · Cited by 36 · see citing works
Self-citationGalili, E., Gopher, A., Eshed, V., & Hershkovitz, I. (2005) · Bulletin of the American Schools of Oriental Research · doi:10.1086/basor25066900 · Cited by 33 · see citing works
Self-citationTaylor, G. M., Stewart, G. R., Cooke, M., Chaplin, S., Ladva, S., Kirkup, J., Palmer, S., & Young, D. (2003) · Microbiology · doi:10.1099/mic.0.26654-0 · Cited by 31 · see citing works
Rothschild, B. M., & Martin, L. D. (2011) · Reumatismo · doi:10.4081/reumatismo.2003.58 · Cited by 28 · see citing works
Palaeobacteriology With Special Reference to Pathogenic Mycobacteria
Spigelman, M., & Donoghue, H. D. (2003) · doi:10.1093/oso/9780198509004.003.0015 · Cited by 11 · see citing works
Self-citationMTB complex DNA in a Scandinavian Neolithic passage grave
Nuorala, E., Götherström, A., Ahlström, T., Donoghue, H. D., Spigelman, M., & Lidén, K. (2004) · UCL Discovery (University College London) · Cited by 7 · see citing works
Self-citation
Flagged first, then by citations
Cited by
Sorted by citations
Boivin, N. L., Zeder, M. A., Fuller, D. Q., Crowther, A., Larson, G., Erlandson, J. M., Denham, T., & Petraglia, M. D. (2016) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1525200113 · Cited by 837 · see citing works
Ecology and evolution of Mycobacterium tuberculosis
Gagneux, S. (2018) · Nature Reviews Microbiology · doi:10.1038/nrmicro.2018.8 · Cited by 618 · see citing works
Extra Pulmonary Tuberculosis: An Overview
Cantres-Fonseca, O. J., Rodríguez-Cintrón, W., Olmo-Arroyo, F. D., & Baez-Corujo, S. (2019) · IntechOpen eBooks · doi:10.5772/intechopen.81322 · Cited by 517 · see citing works
Co‐evolution of M ycobacterium tuberculosis and H omo sapiens
Brites, D., & Gagneux, S. (2015) · Immunological Reviews · doi:10.1111/imr.12264 · Cited by 317 · see citing works
Archaeological and Anthropological Sciences
(2013) · Archaeological and Anthropological Sciences · doi:10.1007/12520.1866-9565 · Cited by 270 · see citing works
Tuberculosis: Current situation, challenges and overview of its control programs in India
Sandhu, G. (2011) · Journal of Global Infectious Diseases · doi:10.4103/0974-777x.81691 · Cited by 261 · see citing works
Genomic insights into tuberculosis
Galagan, J. E. (2014) · Nature Reviews Genetics · doi:10.1038/nrg3664 · Cited by 251 · see citing works
Mycobacterium tuberculosis Dissemination Plays a Critical Role in Pathogenesis
Moule, M. G., & Cirillo, J. D. (2020) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2020.00065 · Cited by 244 · see citing works
Tuberculosis, Pulmonary Cavitation, and Matrix Metalloproteinases
Ong, C. W. M., Elkington, P. T., & Friedland, J. S. (2014) · American Journal of Respiratory and Critical Care Medicine · doi:10.1164/rccm.201311-2106pp · Cited by 240 · see citing works
Barreiro, L. B., Tailleux, L., Pai, A. A., Gicquel, B., Marioni, J. C., & Gilad, Y. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1115761109 · Cited by 239 · see citing works
Myths and misconceptions: the origin and evolution of Mycobacterium tuberculosis
Smith, N. H., Hewinson, R. G., Kremer, K., Brosch, R., & Gordon, S. V. (2009) · Nature Reviews Microbiology · doi:10.1038/nrmicro2165 · Cited by 229 · see citing works
Steps towards the discovery of Mycobacterium tuberculosis by Robert Koch, 1882
Cambau, E., & Drancourt, M. (2014) · Clinical Microbiology and Infection · doi:10.1111/1469-0691.12555 · Cited by 223 · see citing works
Kay, G. L., Sergeant, M. J., Zhou, Z., Chan, J. Z.-M., Millard, A. D., Quick, J., Szikossy, I., Pap, I., Spigelman, M., Loman, N. J., et al. (2015) · Nature Communications · doi:10.1038/ncomms7717 · Cited by 198 · see citing works
Self-citationTuberculosis origin: The Neolithic scenario
Hershkovitz, I., Donoghue, H. D., Minnikin, D. E., May, H., Lee, O. Y.-C., Feldman, M., Galili, E., Spigelman, M., Rothschild, B. M., & Bar‐Gal, G. K. (2015) · Tuberculosis · doi:10.1016/j.tube.2015.02.021 · Cited by 174 · see citing works
Self-citationQ&A: What are pathogens, and what have they done to and for us?
Balloux, F., & van Dorp, L. (2017) · BMC Biology · doi:10.1186/s12915-017-0433-z · Cited by 154 · see citing works
Tuberculosis Drug Discovery: Challenges and New Horizons
Fernandes, G., Thompson, A. M., Castagnolo, D., Denny, W. A., & dos Santos, J. L. (2022) · Journal of Medicinal Chemistry · doi:10.1021/acs.jmedchem.2c00227 · Cited by 153 · see citing works
Tracing hepatitis B virus to the 16th century in a Korean mummy
Bar‐Gal, G. K., Kim, M. J., Klein, A., Shin, D. H., Oh, C. S., Kim, J. W., Kim, T. H., Kim, S. B., Grant, P. R., Pappo, O., et al. (2012) · Hepatology · doi:10.1002/hep.25852 · Cited by 148 · see citing works
Self-citationThe molecular clock of Mycobacterium tuberculosis
Menardo, F., Duchêne, S., Brites, D., & Gagneux, S. (2019) · PLoS Pathogens · doi:10.1371/journal.ppat.1008067 · Cited by 144 · see citing works
Blouin, Y., Hauck, Y., Soler, C., Fabre, M., Vong, R., Dehan, C., Cazajous, G., Massoure, P., Kraemer, P., Jenkins, A. O., et al. (2012) · PLoS ONE · doi:10.1371/journal.pone.0052841 · Cited by 132 · see citing works
Health status and quality of life in tuberculosis
Brown, J., Capocci, S., Smith, C. J., Stephen Morris, A., Abubakar, I. I., & Lipman, M. C. I. (2015) · International Journal of Infectious Diseases · doi:10.1016/j.ijid.2014.12.045 · Cited by 128 · see citing works
Infection, Disease, and Biosocial Processes at the End of the Indus Civilization
Schug, G. R., Blevins, K. E., Cox, B., Gray, K. M., & Mushrif‐Tripathy, V. (2013) · PLoS ONE · doi:10.1371/journal.pone.0084814 · Cited by 124 · see citing works
PET/CT imaging of Mycobacterium tuberculosis infection
Ankrah, A. O., van der Werf, T. S., de Vries, E. F. J., Dierckx, R., Sathekge, M. M., & Glaudemans, A. W. J. M. (2016) · Clinical and Translational Imaging · doi:10.1007/s40336-016-0164-0 · Cited by 124 · see citing works
Tuberculosis and leprosy in perspective
Stone, A. C., Wilbur, A. K., Buikstra, J. E., & Roberts, C. A. (2009) · American Journal of Physical Anthropology · doi:10.1002/ajpa.21185 · Cited by 121 · see citing works
Paleopathology and the origin of agriculture in the Levant
Eshed, V., Gopher, A., Pinhasi, R., & Hershkovitz, I. (2010) · American Journal of Physical Anthropology · doi:10.1002/ajpa.21301 · Cited by 116 · see citing works
Self-citationMycobacterium tuberculosis Transmission in High-Incidence Settings—New Paradigms and Insights
Coleman, M. C., Martínez, L., Theron, G., Wood, R., & Marais, B. J. (2022) · Pathogens · doi:10.3390/pathogens11111228 · Cited by 115 · see citing works
Actinobacteria: the good, the bad, and the ugly
Miao, V., & DAVIES, J. E. (2010) · Antonie van Leeuwenhoek · doi:10.1007/s10482-010-9440-6 · Cited by 114 · see citing works
Page, A. E., Viguier, S., Dyble, M., Major‐Smith, D., Chaudhary, N., Salalι, G. D., Thompson, J., Vinicius, L., Mace, R. H., & Migliano, A. B. (2016) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1524031113 · Cited by 113 · see citing works
Donoghue, H. D., Lee, O. Y.-C., Minnikin, D. E., Besra, G. S., Taylor, J. H., & Spigelman, M. (2009) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2009.1484 · Cited by 112 · see citing works
Self-citationHistory of Pulmonary Tuberculosis
Pezzella, A. T. (2018) · Thoracic surgery clinics/Thorac. surg. clin. · doi:10.1016/j.thorsurg.2018.09.002 · Cited by 111 · see citing works
An update on the role of 18F-FDG-PET/CT in major infectious and inflammatory diseases.
Kung, B. T., Seraj, S. M., Zadeh, M. Z., Rojulpote, C., Kothekar, E., Ayubcha, C., Ng, K. S., Ng, K. K., Au-Yong, T. K., Werner, T. J., et al. (2019) · Europe PMC (PubMed Central) · Cited by 108 · see citing works
Antimicrobial Resistance in Mycobacterium tuberculosis : The Odd One Out
Eldholm, V., & Balloux, F. (2016) · Trends in Microbiology · doi:10.1016/j.tim.2016.03.007 · Cited by 104 · see citing works
Nicklisch, N., Maixner, F., Ganslmeier, R., Friederich, S., Dresely, V., Meller, H., Zink, A., & Alt, K. W. (2012) · American Journal of Physical Anthropology · doi:10.1002/ajpa.22137 · Cited by 100 · see citing works
Lazzeri, E., Bozzao, A., Cataldo, M. A., Petrosillo, N., Manfrè, L., Trampuž, A., Signore, A., & Muto, M. (2019) · European Journal of Nuclear Medicine and Molecular Imaging · doi:10.1007/s00259-019-04393-6 · Cited by 99 · see citing works
Schultz, F., Anywar, G., Wack, B., Quave, C. L., & Garbe, L. (2020) · Journal of Ethnopharmacology · doi:10.1016/j.jep.2020.112742 · Cited by 98 · see citing works
Sabin, S. J., Herbig, A., Vågene, Å. J., Ahlström, T., Božović, G., Arcini, C., Kühnert, D., & Bos, K. I. (2020) · Genome biology · doi:10.1186/s13059-020-02112-1 · Cited by 97 · see citing works
The role of hydrophobicity in tuberculosis evolution and pathogenicity
Jankute, M., Nataraj, V., Lee, O. Y.-C., Wu, H. H. T., Ridell, M., Garton, N. J., Barer, M. R., Minnikin, D. E., Bhatt, A., & Besra, G. S. (2017) · Scientific Reports · doi:10.1038/s41598-017-01501-0 · Cited by 96 · see citing works
Self-citationHuman tuberculosis predates domestication in ancient Syria
Baker, O., Lee, O. Y.-C., Wu, H. H. T., Besra, G. S., Minnikin, D. E., Llewellyn, G., Williams, C. M., Maixner, F., O’Sullivan, N. J., Zink, A., et al. (2015) · Tuberculosis · doi:10.1016/j.tube.2015.02.001 · Cited by 96 · see citing works
Self-citationMancuso, G., Midiri, A., Gaetano, S. D., Ponzo, E., & Biondo, C. (2023) · Microorganisms · doi:10.3390/microorganisms11092277 · Cited by 95 · see citing works
Evolution of human tuberculosis: A systematic review and meta-analysis of paleopathological evidence
Holloway‐Kew, K. L., Henneberg, R. J., Lopes, M. D. B., & Henneberg, M. (2011) · HOMO · doi:10.1016/j.jchb.2011.10.001 · Cited by 90 · see citing works
Masson, M., Molnár, E., Donoghue, H. D., Besra, G. S., Minnikin, D. E., Wu, H. H. T., Lee, O. Y.-C., Bull, I. D., & Pálfi, G. (2013) · PLoS ONE · doi:10.1371/journal.pone.0078252 · Cited by 89 · see citing works
Self-citationThe Nature and Evolution of Genomic Diversity in the Mycobacterium tuberculosis Complex
Brites, D., & Gagneux, S. (2017) · Advances in experimental medicine and biology · doi:10.1007/978-3-319-64371-7_1 · Cited by 88 · see citing works
Mycobacterium tuberculosis progresses through two phases of latent infection in humans
Colangeli, R., Gupta, A., Vinhas, S. A., Venkata, U. D. C., Kim, S., Grady, C. A., Jones‐López, E. C., Soteropoulos, P., Palaci, M., Marques-Rodrigues, P., et al. (2020) · Nature Communications · doi:10.1038/s41467-020-18699-9 · Cited by 86 · see citing works
Mycobacterial Musculoskeletal Infections
Hogan, J. I., Hurtado, R. M., & Nelson, S. B. (2017) · Infectious Disease Clinics of North America · doi:10.1016/j.idc.2017.01.007 · Cited by 84 · see citing works
Deficiencies and challenges in the study of ancient tuberculosis DNA
Wilbur, A. K., Bouwman, A., Stone, A. C., Roberts, C. A., Pfister, L., Buikstra, J. E., & Brown, T. A. (2009) · Journal of Archaeological Science · doi:10.1016/j.jas.2009.05.020 · Cited by 83 · see citing works
Anastasiou, E., & Mitchell, P. D. (2013) · Gene · doi:10.1016/j.gene.2013.06.017 · Cited by 82 · see citing works
Lee, O. Y.-C., Wu, H. H. T., Donoghue, H. D., Spigelman, M., Greenblatt, C. L., Bull, I. D., Rothschild, B. M., Martin, L. D., Minnikin, D. E., & Besra, G. S. (2012) · PLoS ONE · doi:10.1371/journal.pone.0041923 · Cited by 82 · see citing works
Self-citationXu, C., Xu, J. Y., Chen, Y., Wu, R., Ji, H., Pan, Y., Duan, Y., Sun, M., Du, L., Gao, M., et al. (2021) · Scientific Reports · doi:10.1038/s41598-021-03811-w · Cited by 79 · see citing works
How should we diagnose disease in palaeopathology? Some epistemological considerations
Mays, S. A. (2017) · International Journal of Paleopathology · doi:10.1016/j.ijpp.2017.10.006 · Cited by 79 · see citing works
A Color Atlas of Comparative Pathology of Pulmonary Tuberculosis
(2010) · CRC Press eBooks · doi:10.1201/ebk1439835272 · Cited by 76 · see citing works
Osteological and molecular identification of brucellosis in ancient Butrint, Albania
Mutolo, M. J., Jenny, L., Buszek, A. R., Fenton, T. W., & Foran, D. R. (2011) · American Journal of Physical Anthropology · doi:10.1002/ajpa.21643 · Cited by 72 · see citing works
Drug Treatment of Haemorrhoids
Misra, M. C., & Imlitemsu (2005) · Drugs · doi:10.2165/00003495-200565110-00003 · Cited by 71 · see citing works
Chemical Synthesis of Cell Wall Constituents of Mycobacterium tuberculosis
Holzheimer, M., Buter, J., & Minnaard, A. J. (2021) · Chemical Reviews · doi:10.1021/acs.chemrev.1c00043 · Cited by 70 · see citing works
Molecular Exploration of the First-Century Tomb of the Shroud in Akeldama, Jerusalem
Matheson, C. D., Vernon, K. K., Lahti, A., Fratpietro, R., Spigelman, M., Gibson, S., Greenblatt, C. L., & Donoghue, H. D. (2009) · PLoS ONE · doi:10.1371/journal.pone.0008319 · Cited by 68 · see citing works
Self-citationHuman tuberculosis – an ancient disease, as elucidated by ancient microbial biomolecules
Donoghue, H. D. (2009) · Microbes and Infection · doi:10.1016/j.micinf.2009.08.008 · Cited by 68 · see citing works
Self-citationMycocerosic acid biomarkers for the diagnosis of tuberculosis in the Coimbra Skeletal Collection
Redman, J. E., Shaw, M. J., Mallet, A. I., Santos, A. L., Roberts, C. A., Gernaey, A. M., & Minnikin, D. E. (2009) · Tuberculosis · doi:10.1016/j.tube.2009.04.001 · Cited by 67 · see citing works
Self-citationEvolution of Mycobacterium tuberculosis drug resistance in the genomic era
Nimmo, C., Millard, J., Faulkner, V., Monteserin, J., Pugh, H., & Johnson, E. O. (2022) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2022.954074 · Cited by 64 · see citing works
Multiple Origins of Agriculture in Eurasia and Africa
Bar‐Yosef, O. (2016) · Elsevier eBooks · doi:10.1016/b978-0-12-420190-3.00019-3 · Cited by 63 · see citing works
Research and development of new tuberculosis vaccines: a review
Schrager, L. K., Harris, R. C., & Vekemans, J. (2018) · F1000Research · doi:10.12688/f1000research.16521.2 · Cited by 63 · see citing works
Ancient pathogen genomics: insights into timing and adaptation
Harkins, K. M., & Stone, A. C. (2014) · Journal of Human Evolution · doi:10.1016/j.jhevol.2014.11.002 · Cited by 61 · see citing works
Detection and Strain Typing of Ancient Mycobacterium leprae from a Medieval Leprosy Hospital
Taylor, G. M., Tucker, K., Butler, R. E., Pike, A. W. G., Lewis, J., Roffey, S., Marter, P., Lee, O. Y.-C., Wu, H. H. T., Minnikin, D. E., et al. (2013) · PLoS ONE · doi:10.1371/journal.pone.0062406 · Cited by 61 · see citing works
Self-citationControlled fire use in early humans might have triggered the evolutionary emergence of tuberculosis
Chisholm, R. H., Trauer, J. M., Curnoe, D., & Tanaka, M. M. (2016) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1603224113 · Cited by 61 · see citing works
Diacon, A. H., Barry, C. E., Carlton, A., Chen, R. Y., Davies, M., Jager, V. R. D., Fletcher, K., Koh, G. C. K. W., Kontsevaya, I., Heyckendorf, J., et al. (2024) · Nature Medicine · doi:10.1038/s41591-024-02829-7 · Cited by 60 · see citing works
Shaler, C. R., Horvath, C. N., Lai, R., & Xing, Z. (2012) · Clinical and Developmental Immunology · doi:10.1155/2012/628293 · Cited by 58 · see citing works
The Evolutionary History, Demography, and Spread of the Mycobacterium tuberculosis Complex
Barbier, M., & Wirth, T. (2016) · Microbiology Spectrum · doi:10.1128/microbiolspec.tbtb2-0008-2016 · Cited by 58 · see citing works
Chowdhury, K., Ahmad, R., Sinha, S., Dutta, S., & Haque, M. (2023) · Cureus · doi:10.7759/cureus.35154 · Cited by 56 · see citing works
Has Molecular Docking Ever Brought us a Medicine?
Phillips, M. A., Stewart, M. A., Woodling, D. L., & Xie, Z. (2018) · InTech eBooks · doi:10.5772/intechopen.72898 · Cited by 56 · see citing works
Taylor, G. M., Blau, S., Mays, S. A., Monot, M., Lee, O. Y.-C., Minnikin, D. E., Besra, G. S., Cole, S. T., & Rutland, P. (2009) · Journal of Archaeological Science · doi:10.1016/j.jas.2009.06.026 · Cited by 54 · see citing works
Self-citation7000 year-old tuberculosis cases from Hungary – Osteological and biomolecular evidence
Masson, M., Bereczki, Z., Molnár, E., Donoghue, H. D., Minnikin, D. E., Lee, O. Y.-C., Wu, H. H. T., Besra, G. S., Bull, I. D., & Pálfi, G. (2015) · Tuberculosis · doi:10.1016/j.tube.2015.02.007 · Cited by 54 · see citing works
Self-citationPalaeogenomics of Mycobacterium tuberculosis: epidemic bursts with a degrading genome
Djelouadji, Z., Raoult, D., & Drancourt, M. (2011) · The Lancet Infectious Diseases · doi:10.1016/s1473-3099(11)70093-7 · Cited by 54 · see citing works
Ancient mycobacterial lipids: Key reference biomarkers in charting the evolution of tuberculosis
Minnikin, D. E., Lee, O. Y.-C., Wu, H. H. T., Besra, G. S., Bhatt, A., Nataraj, V., Rothschild, B. M., Spigelman, M., & Donoghue, H. D. (2015) · Tuberculosis · doi:10.1016/j.tube.2015.02.009 · Cited by 53 · see citing works
Self-citationMycobacterial Evolution Intersects With Host Tolerance
Saelens, J. W., Viswanathan, G., & Tobin, D. M. (2019) · Frontiers in Immunology · doi:10.3389/fimmu.2019.00528 · Cited by 52 · see citing works
Paleopathology of Human Tuberculosis and the Potential Role of Climate
Nerlich, M. L., & Lösch, S. (2009) · Interdisciplinary Perspectives on Infectious Diseases · doi:10.1155/2009/437187 · Cited by 51 · see citing works
Lemmer, Y., Kalombo, L., Pietersen, R., Jones, A. T., Semete‐Makokotlela, B., Wyngaardt, S. V., Ramalapa, B., Stoltz, A. C., Baker, B., Verschoor, J. A., et al. (2015) · Journal of Controlled Release · doi:10.1016/j.jconrel.2015.06.005 · Cited by 50 · see citing works
Tuberculosis in Late Neolithic-Early Copper Age human skeletal remains from Hungary
Pósa, A., Maixner, F., Mende, B. G., Köhler, K., Osztás, A., Sola, C., Dutour, O., Masson, M., Molnár, E., Pálfi, G., et al. (2015) · Tuberculosis · doi:10.1016/j.tube.2015.02.011 · Cited by 50 · see citing works
A Late Neolithic Case of Pott's Disease from Hungary
Köhler, K., Pálfi, G., Molnár, E., Zalai-Gaál, I., Osztás, A., Bánffy, E., Kirinó, K., Kiss, K. K., & Mende, B. G. (2012) · International Journal of Osteoarchaeology · doi:10.1002/oa.2254 · Cited by 49 · see citing works
The association between skeletal lesions and tuberculosis diagnosis using a probabilistic approach
Pedersen, D. D., Milner, G. R., Kolmos, H. J., & Boldsen, J. L. (2019) · International Journal of Paleopathology · doi:10.1016/j.ijpp.2019.01.001 · Cited by 49 · see citing works
Insights gained from palaeomicrobiology into ancient and modern tuberculosis
Donoghue, H. D. (2011) · Clinical Microbiology and Infection · doi:10.1111/j.1469-0691.2011.03554.x · Cited by 48 · see citing works
Self-citationGenotyping of ancientMycobacterium tuberculosisstrains reveals historic genetic diversity
Müller, R., Roberts, C. A., & Brown, T. A. (2014) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2013.3236 · Cited by 48 · see citing works
Non-human sources of Mycobacterium tuberculosis
Ghodbane, R., & Drancourt, M. (2013) · Tuberculosis · doi:10.1016/j.tube.2013.09.005 · Cited by 46 · see citing works
Müller, R., Roberts, C. A., & Brown, T. A. (2013) · American Journal of Physical Anthropology · doi:10.1002/ajpa.22417 · Cited by 46 · see citing works
Inskip, S. A., Taylor, G. M., Zakrzewski, S., Mays, S. A., Pike, A. W. G., Llewellyn, G., Williams, C. M., Lee, O. Y.-C., Wu, H. H. T., Minnikin, D. E., et al. (2015) · PLoS ONE · doi:10.1371/journal.pone.0124282 · Cited by 46 · see citing works
Self-citationBeyond ancient microbial DNA: Nonnucleotidic Biomolecules For Paleomicrobiology
Tran, T.-N.-N., Aboudharam, G., Raoult, D., & Drancourt, M. (2011) · BioTechniques · doi:10.2144/000113689 · Cited by 45 · see citing works
The challenge of identifying tuberculosis proteins in archaeological tissues
Hendy, J., Collins, M. J., Teoh, K. Y., Ashford, D. A., THOMAS‐OATES, J. E., Donoghue, H. D., Pap, I., Minnikin, D. E., Spigelman, M., & Buckley, M. (2016) · Journal of Archaeological Science · doi:10.1016/j.jas.2016.01.003 · Cited by 45 · see citing works
Self-citationPaleomicrobiology of Human Tuberculosis
Donoghue, H. D. (2016) · Microbiology Spectrum · doi:10.1128/microbiolspec.poh-0003-2014 · Cited by 45 · see citing works
Self-citationDomesticating gender: Neolithic patterns from the southern Levant
Peterson, J. (2010) · Journal of Anthropological Archaeology · doi:10.1016/j.jaa.2010.03.002 · Cited by 44 · see citing works
Sudden cardiac death and tuberculosis – How much do we know?
Liu, A., Hu, Y., & Coates, A. R. M. (2012) · Tuberculosis · doi:10.1016/j.tube.2012.02.002 · Cited by 44 · see citing works
Minnikin, D. E., Lee, O. Y.-C., Wu, H. H. T., Nataraj, V., Donoghue, H. D., Ridell, M., Watanabe, M., Alderwick, L., Bhatt, A., & Besra, G. S. (2015) · Tuberculosis - Expanding Knowledge · doi:10.5772/59585 · Cited by 43 · see citing works
Self-citationDonoghue, H. D., Spigelman, M., O’Grady, J., Szikossy, I., Pap, I., Lee, O. Y.-C., Wu, H. H. T., Besra, G. S., & Minnikin, D. E. (2015) · Tuberculosis · doi:10.1016/j.tube.2015.02.020 · Cited by 43 · see citing works
Self-citationGenetic Diversity of Toll-Like Receptors and Immunity toM. lepraeInfection
Hart, B. E., & Tapping, R. I. (2012) · Journal of Tropical Medicine · doi:10.1155/2012/415057 · Cited by 43 · see citing works
Spigelman, M., Donoghue, H. D., Abdeen, Z., Ereqat, S., Sarie, I., Greenblatt, C. L., Pap, I., Szikossy, I., Hershkovitz, I., Bar‐Gal, G. K., et al. (2015) · Tuberculosis · doi:10.1016/j.tube.2015.02.022 · Cited by 42 · see citing works
Self-citationThe The paleopathological evidence on the origins of human tuberculosis: a review
Ileana, B., & Giuffra, V. (2019) · Journal of preventive medicine and hygiene · doi:10.15167/2421-4248/jpmh2020.61.1s1.1379 · Cited by 42 · see citing works
Identification of a Desaturase Involved in Mycolic Acid Biosynthesis in Mycobacterium smegmatis
Singh, A., Varela, C., Bhatt, K., Veerapen, N., Lee, O. Y.-C., Wu, H. H. T., Besra, G. S., Minnikin, D. E., Fujiwara, N., Teramoto, K., et al. (2016) · PLoS ONE · doi:10.1371/journal.pone.0164253 · Cited by 42 · see citing works
Self-citationA review of tuberculosis: Focus on bedaquiline
Chan, B., Khadem, T. M., & Brown, J. E. (2013) · American Journal of Health-System Pharmacy · doi:10.2146/ajhp130199 · Cited by 41 · see citing works
Neonate Human Remains: A Window of Opportunity to the Molecular Study of Ancient Syphilis
Montiel, R., Eduvigis Solórzano, N., Díaz, N., Álvarez-Sandoval, B. A., González‐Ruiz, M., Cañadas, M. P., Simões, N., Isidro, A., & Morera, A. M. (2012) · PLoS ONE · doi:10.1371/journal.pone.0036371 · Cited by 40 · see citing works
New perspectives in biomolecular paleopathology of ancient tuberculosis: a proteomic approach
Boros-Major, A., Bóna, Á., Lovasz, G., Molnár, E., Marcsik, A., Pálfi, G., & Márk, L. (2010) · Journal of Archaeological Science · doi:10.1016/j.jas.2010.09.008 · Cited by 40 · see citing works
Sex and Gender Differences in Tuberculosis Pathogenesis and Treatment Outcomes
Dabitao, D., & Bishai, W. R. (2023) · Current topics in microbiology and immunology · doi:10.1007/978-3-031-35139-6_6 · Cited by 39 · see citing works
Šimonovičová, A., Kraková, L., Pangallo, D., Majorošová, M., Piecková, E., Bodoríková, S., & Dörnhöferová, M. (2015) · International Biodeterioration & Biodegradation · doi:10.1016/j.ibiod.2014.12.011 · Cited by 39 · see citing works
The Bioarchaeology of Health Crisis: Infectious Disease in the Past
Larsen, C. S. (2018) · Annual Review of Anthropology · doi:10.1146/annurev-anthro-102116-041441 · Cited by 39 · see citing works
Skeletal Lesions in Human Tuberculosis May Sometimes Heal: An Aid to Palaeopathological Diagnoses
Holloway‐Kew, K. L., Link, K., Rühli, F. J., & Henneberg, M. (2013) · PLoS ONE · doi:10.1371/journal.pone.0062798 · Cited by 38 · see citing works
Lipid biomarkers provide evolutionary signposts for the oldest known cases of tuberculosis
Lee, O. Y.-C., Wu, H. H. T., Besra, G. S., Rothschild, B. M., Spigelman, M., Hershkovitz, I., Bar‐Gal, G. K., Donoghue, H. D., & Minnikin, D. E. (2015) · Tuberculosis · doi:10.1016/j.tube.2015.02.013 · Cited by 38 · see citing works
Self-citation
- Authors
- Hershkovitz, I., Donoghue, H. D., Minnikin, D. E., Besra, G. S., Lee, O. Y.-C., Gernaey, A. M., Galili, E., Eshed, V., Greenblatt, C. L., Lemma, E., Bar-Gal, G. K., & Spigelman, M.
- Affiliations
- University College London (GB)
- University of Birmingham (GB)
- University of Salford (GB)
- Israel Antiquities Authority (IL)
- Tel Aviv University (IL)
- Hebrew University of Jerusalem (IL)
- Corresponding author
- Donoghue, Helen D.
- ORCID
- Venue
- PLoS ONE
- Publisher
- Public Library of Science (PLoS)
- Published
- 2008-10-15
- Volume
- 3
- Issue
- 10
- Pages
- e3426
- ISSN
- 1932-6203 (ISSN-L)
- PMC
- PMC2565837
- OpenAlex
- W2052515110
- Cited by
- 506
- References
- 51
- Citations by year
- 2026: 11 · 2025: 13 · 2024: 26 · 2023: 37 · 2022: 30 · 2021: 30 · 2020: 29 · 2019: 42 · 2018: 30 · 2017: 39 · 2016: 40 · 2015: 33 · 2014: 26 · 2013: 36 · 2012: 25
- FWCI
- 167.98
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- PLoS ONE (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- UCL Discovery (University College London) (submittedVersion)
- Figshare (submittedVersion, cc-by)
- University of Birmingham Research Portal (University of Birmingham) (submittedVersion, other-oa)
- Funders
- Leverhulme Trust
- Deutsche Forschungsgemeinschaft
- Dan David Prize
- Topics
- Social Sciences › Arts and Humanities › Archeology › Paleopathology and ancient diseases
- Health Sciences › Medicine › Infectious Diseases › Tuberculosis Research and Epidemiology
- Physical Sciences › Earth and Planetary Sciences › Paleontology › Archaeology and ancient environmental studies
- Keywords
- Mycobacterium tuberculosis, Neolithic, ancient DNA, host-pathogen coevolution, tuberculosis transmission, animal domestication, human remains, Eastern Mediterranean
- MeSH terms
- Adult, Bone and Bones, DNA, Bacterial, Female, Humans, Infant, Mycobacterium tuberculosis, Tuberculosis, Polymerase Chain Reaction, Mediterranean Region, History, Ancient
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review