1887

Abstract

Tuberculosis has plagued humankind since prehistoric times, as is evident from characteristic lesions on human skeletons dating back to the Neolithic period. The disease in man is due predominantly to infection with either or , both members of the (MTB) complex. A number of studies have shown that when conditions permit, surviving mycobacterial DNA may be amplified from bone by PCR. Such ancient DNA (aDNA) analyses are subject to stringent tests of authenticity and, when feasible, are invariably limited by DNA fragmentation. Using PCRs based on single-nucleotide polymorphic loci and regions of difference (RDs) in the MTB complex, a study was made of five Iron Age individuals with spinal lesions recovered from the cemetery of Aymyrlyg, South Siberia. A sensitive screening PCR for MTB complex mycobacteria was positive in four out of the five cases. Genotyping evidence indicated that all four cases were due to infection with rather than and the data were consistent with the proposed phylogenetic model of the MTB complex. This is believed to be the first report of causing Pott's disease in archaeological human remains. The study shows that genotyping of ancestral strains of MTB complex mycobacteria from contexts of known date provides information which allows the phylogeny of the model to be tested. Moreover, it shows that loss of DNA from RD4, which defines classic , had already occurred from the genome over 2000 years before the present.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.2006/002154-0
2007-04-01
2019-10-21
Loading full text...

Full text loading...

/deliver/fulltext/micro/153/4/1243.html?itemId=/content/journal/micro/10.1099/mic.0.2006/002154-0&mimeType=html&fmt=ahah

References

  1. Aranaz, A., Cousins, D., Mateos, A. & Dominguez, L. ( 2003; ). Elevation of Mycobacterium tuberculosis subsp. caprae Aranaz et al., 1999 to species rank as Mycobacterium caprae comb. nov., sp. nov. Int J Syst Evol Microbiol 53, 1785–1789.[CrossRef]
    [Google Scholar]
  2. Behr, M. A., Wilson, M. A., Gill, W. P., Salamon, H., Schoolnik, G. K., Rane, S. & Small, P. ( 1999; ). Comparative genomics of BCG vaccines by whole-genome DNA microarray. Science 284, 1520–1523.[CrossRef]
    [Google Scholar]
  3. Bronk-Ramsey, C. ( 2000; ). OxCal v3.5 program. Available at http://c14.arch.ox.ac.uk/oxcal/OxCalPlot.html
  4. Brosch, R., Gordon, S. V., Marmiesse, M., Brodin, P., Buchrieser, C., Eiglmeier, K., Garnier, T., Gutierrez, C., Hewinson, G. & other authors ( 2002; ). A new evolutionary scenario for the Mycobacterium tuberculosis complex. Proc Natl Acad Sci U S A 99, 3684–3689.[CrossRef]
    [Google Scholar]
  5. Buikstra, J. E. & Ubelaker, D. H. ( 1994; ). Standards for Data Collection from Human Skeletal Remains. Research Series no. 44. Fayetteville: Arkansas Archaeological Survey Press.
  6. Cano, R. J. ( 1996; ). Analysing ancient DNA. Endeavour 20, 162–167.[CrossRef]
    [Google Scholar]
  7. Collins, D. M. & Stephens, D. M. ( 1991; ). Identification of an insertion sequence, IS1081, in Mycobacterium bovis. FEMS Microbiol Lett 67, 11–15.
    [Google Scholar]
  8. Cotter, T. P., O'Shaughnessy, E., Sheehan, S., Cryan, B. & Bredin, C. P. ( 1996; ). Human Mycobacterium bovis infection in the south-west of Ireland 1983–1992: a comparison with M. tuberculosis. Ir Med J 89, 62–63.
    [Google Scholar]
  9. Donoghue, H. D., Spigelman, M., Greenblatt, C. L., Lev-Maor, G., Bar-Gal, G. K., Matheson, C., Vernon, K., Nerlick, A. G. & Zink, A. R. ( 2004; ). Tuberculosis: from prehistory to Robert Koch, as revealed by ancient DNA. Lancet Infect Dis 4, 584–592.[CrossRef]
    [Google Scholar]
  10. Dziadek, J., Sajduda, A. & Borun, T. M. ( 2001; ). Specificity of insertion sequence-based PCR assays for Mycobacterium tuberculosis complex. Int J Tuberc Lung Dis 5, 569–574.
    [Google Scholar]
  11. Ferembach, D., Schwidetzky, I. & Stloukal, M. ( 1980; ). Recommendations for age and sex diagnoses of skeletons. J Hum Evol 9, 517–549.[CrossRef]
    [Google Scholar]
  12. Fletcher, H. A., Donoghue, H. D., Taylor, G. M., van der Zanden, A. G. M. & Spigelman, M. ( 2003; ). Molecular analysis of Mycobacterium tuberculosis DNA from a family of 18th century Hungarians. Microbiology 149, 143–151.[CrossRef]
    [Google Scholar]
  13. Gagneux, S., DeReimer, K., Van, T., Kato-Maeda, M., de Jong, B. C., Narayanan, S., Nicol, M., Nieman, S., Kremer, K. & other authors ( 2006; ). Variable host–pathogen compatibility in Mycobacterium tuberculosis. Proc Natl Acad Sci U S A 103, 2869–2873.[CrossRef]
    [Google Scholar]
  14. Gryaznov, M. ( 1969; ). The Ancient Civilization of South Siberia. London: Barrie & Rockliff: the Cresset Press.
  15. Gutierrez, M., Samper, S., Jimenez, M. S., van Embden, J. D., Marin, J. F. & Martin, C. ( 1997; ). Identification by spoligotyping of a caprine genotype in Mycobacterium bovis strains causing human tuberculosis. J Clin Microbiol 35, 3328–3330.
    [Google Scholar]
  16. Gutierrez, M. C., Brisse, S., Brosch, R., Fabre, M., Omais, B., Marmiesse, M., Supply, P. & Vincent, V. ( 2005; ). Ancient origin and gene mosaicism of the progenitor of Mycobacterium tuberculosis. PloS Pathogens 1, 1–7.[CrossRef]
    [Google Scholar]
  17. Haddad, N., Ostyn, A., Karoui, C., Masselot, M., Thorel, M. F., Hughes, S. L., Inwald, J., Hewinson, R. G. & Durand, B. ( 2001; ). Spoligotype diversity of Mycobacterium bovis strains isolated in France from 1979 to 2000. J Clin Microbiol 39, 3623–3632.[CrossRef]
    [Google Scholar]
  18. Hermans, P. W., van Soolingen, D., Bik, E. M., de Haas, P. E., Dale, J. W. & van Embden, J. D. ( 1991; ). Insertion element IS987 from Mycobacterium bovis BCG is located in a hot-spot integration region for insertion elements in Mycobacterium tuberculosis complex strains. Infect Immun 59, 2695–2705.
    [Google Scholar]
  19. Liebana, E., Aranaz, A., Dominguez, L., Mateos, A., Gonzalez-Llamazares, O., Rodriguez-Ferri, E. F., Domingo, M., Vidal, D. & Cousins, D. ( 1997; ). The insertion element IS6110 is a useful tool for DNA fingerprinting of Mycobacterium bovis isolates from cattle and goats in Spain. Vet Microbiol 54, 223–233.[CrossRef]
    [Google Scholar]
  20. LoBue, P. A., Betancourt, W., Cowan, L., Seli, L., Peter, C. & Moser, K. S. ( 2004; ). Identification of a familial cluster of pulmonary Mycobacterium bovis disease. Int J Tuberc Lung Dis 8, 1142–1146.
    [Google Scholar]
  21. Malone, F. E., Wilson, E. C., Pollock, J. M. & Skuce, R. A. ( 2003; ). Investigations into an outbreak of tuberculosis in a flock of sheep in contact with tuberculous cattle. J Vet Med B Infect Dis Vet Public Health 50, 500–504.[CrossRef]
    [Google Scholar]
  22. Mays, S. ( 2005; ). Tuberculosis as a zoonotic disease in antiquity. In Diet and Health in Past Animal Populations: Current Research and Future Directions, pp. 125–134. Edited by J. Davies, M. Fabiš, I. Mainland, M. Richards & R. Thomas. Oxford: Oxbow.
  23. Mays, S. A., Taylor, G. M., Legge, A. J., Young, D. B. & Turner-Walker, G. A. ( 2001; ). Palaeopathological and biomolecular study of tuberculosis in a medieval skeletal collection from England. Am J Phys Anthropol 114, 298–311.[CrossRef]
    [Google Scholar]
  24. Mostowy, S., Inwald, J., Gordon, S., Martin, C., Warren, R., Kremer, K., Cousins, D. & Behr, M. A. ( 2005; ). Revisiting the evolution of Mycobacterium bovis. J Bacteriol 187, 6386–6395.[CrossRef]
    [Google Scholar]
  25. O'Reilly, L. M. & Daborn, C. J. ( 1995; ). The epidemiology of Mycobacterium bovis infections in animals and man: a review. Tuber Lung Dis 76 (suppl. 1), 1–46.
    [Google Scholar]
  26. Ortner, D. J. ( 1999; ). Palaeopathology: implications for the history and evolution of tuberculosis. In Tuberculosis Past and Present, pp. 255–261. Edited by G. Pálfi, O. Dutour, J. Deák & I. Hutás. Budapest: Golden Books/Tuberculosis Foundation.
  27. Ortner, D. J. & Putschar, W. G. J. ( 1985; ). The Identification of Pathological Conditions in Human Skeletal Remains. Washington: Smithsonian Institution Press.
  28. Plikaytis, B. B., Crawford, J. T., Woodley, C. L., Butler, W. R., Eisenach, K. D., Cave, M. D. & Shinnick, T. M. ( 1993; ). Rapid, amplification-based fingerprinting of Mycobacterium tuberculosis. J Gen Microbiol 139, 1537–1542.[CrossRef]
    [Google Scholar]
  29. Roberts, C. A. & Buikstra, J. E. ( 2003; ). The Bioarchaeology of Tuberculosis: a Global View on a Re-emerging Disease. Tampa: University Press of Florida.
  30. Robinson, P., Morris, D. & Antic, R. ( 1988; ). Mycobacterium bovis as an occupational hazard in abattoir workers. Aust N Z J Med 18, 701–703.[CrossRef]
    [Google Scholar]
  31. Scorpio, A., Collins, D., Whipple, D., Cave, D., Bates, J. & Zhang, Y. ( 1997; ). Rapid differentiation of bovine and human tubercle bacilli based on a characteristic mutation in the bovine pyrazinamidase gene. J Clin Microbiol 35, 106–110.
    [Google Scholar]
  32. Smith, R. M., Drobniewski, F., Gibson, A., Montague, J. D., Logan, M. N., Hunt, D., Hewinson, G., Salmon, M. R. & O'Neill, B. ( 2004; ). Mycobacterium bovis infection, United Kingdom. Emerg Infect Dis 10, 539–541.[CrossRef]
    [Google Scholar]
  33. Sreevatsan, S., Escalante, P., Pan, X., Gillies, D. A., Siddiqui, S., Khalaf, C. N., Kreiswirth, B. N., Bifani, P. & Adams, L. G. ( 1996; ). Identification of a polymorphic nucleotide in oxyR specific for Mycobacterium bovis. J Clin Microbiol 34, 2007–2010.
    [Google Scholar]
  34. Sreevatsan, S., Pan, X., Stockbauer, K. E., Connell, N. D., Kreiswirth, B. N., Whitman, S. & Musser, J. M. ( 1997; ). Restricted structural gene polymorphism in the Mycobacterium tuberculosis complex indicates evolutionarily recent global dissemination. Proc Natl Acad Sci U S A 94, 9869–9874.[CrossRef]
    [Google Scholar]
  35. Stuiver, M., Reimer, P. J., Bard, E., Beck, J. W., Burr, G. S., Hughen, K. A., Kromer, B., McCormac, G., van der Plicht, J. & Spurk, M. ( 1998; ). INTCAL98 radiocarbon age calibration, 24000-0 cal BP. Radiocarbon 40, 1041–1083.
    [Google Scholar]
  36. Sun, Y. J., Lee, A. S., Ng, S. T., Ravindran, S., Kremer, K., Bellamy, R., Wong, S. Y., van Soolingen, D., Supply, P. & Paton, N. I. ( 2004; ). Characterization of ancestral Mycobacterium tuberculosis by multiple genetic markers and proposal of genotyping strategy. J Clin Microbiol 42, 5058–5064.[CrossRef]
    [Google Scholar]
  37. Taylor, G. M., Goyal, M., Legge, A. J., Shaw, R. J. & Young, D. ( 1999; ). Genotypic analysis of Mycobacterium tuberculosis from medieval human remains. Microbiology 145, 899–904.[CrossRef]
    [Google Scholar]
  38. Taylor, G. M., Stewart, G. R., Cooke, M., Chaplin, S., Ladva, S., Kirkup, J., Palmer, S. & Young, D. B. ( 2003; ). Koch's Bacillus – a look at the first isolate of Mycobacterium tuberculosis from a modern perspective. Microbiology 149, 3213–3220.[CrossRef]
    [Google Scholar]
  39. Taylor, G. M., Young, D. B. & Mays, S. A. ( 2005; ). Genotypic analysis of the earliest known prehistoric case of tuberculosis in Britain. J Clin Microbiol 43, 2236–2240.[CrossRef]
    [Google Scholar]
  40. Taylor, G. M., Watson, C. L., Bouwman, A. S., Lockwood, D. N. J. & Mays, S. A. ( 2006; ). Variable nucleotide tandem repeat (VNTR) typing of two palaeopathological cases of lepromatous leprosy from Mediaeval England. J Arch Sci 33, 1569–1579.[CrossRef]
    [Google Scholar]
  41. Thompson, P. J., Cousins, D. V., Gow, B. L., Collins, D. M., Williamson, B. H. & Dagnia, H. T. ( 1993; ). Seals, seal trainers, and mycobacterial infection. Am Rev Respir Dis 147, 164–167.[CrossRef]
    [Google Scholar]
  42. Vainshtein, S. ( 1980; ). Nomads of South Siberia: the Pastoral Economies of Tuva. Cambridge: Cambridge University Press.
  43. Yuen, L. K., Ross, B. C., Jackson, K. M. & Dwyer, B. ( 1993; ). Characterization of Mycobacterium tuberculosis strains from Vietnamese patients by Southern blot hybridization. J Clin Microbiol 31, 1615–1618.
    [Google Scholar]
  44. Zink, A. R., Sola, C., Reischl, U., Grabner, W., Rastogi, N., Wolf, H. & Nerlich, A. G. ( 2003; ). Characterization of Mycobacterium tuberculosis complex DNAs from Egyptian mummies by spoligotyping. J Clin Microbiol 41, 359–367.[CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.2006/002154-0
Loading
/content/journal/micro/10.1099/mic.0.2006/002154-0
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error