Absence of Yersinia pestis-specific DNA in human teeth from five European excavations of putative plague victims

Microbiology

Volumn 150, Issue 2, 2004, Pages 341-354

  Gilbert, M Thomas P ^a,f   Cuccui, Jon ^b   White, William ^c   Lynnerup, Niels ^d   Titball, Richard W ^e   Cooper, Alan ^a   Prentice, Michael B ^b  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

^c MUSEUM OF LONDON ARCHAEOLOGY   (United Kingdom)

^d UNIVERSITY OF COPENHAGEN   (Denmark)

^e DEFENCE SCIENCE AND TECHNOLOGY LABORATORY   (United Kingdom)

^f UNIVERSITY OF ARIZONA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL DNA; DNA 16S;

ARTICLE; BACTEREMIA; BACTERIUM CONTAMINATION; BACTERIUM IDENTIFICATION; CLINICAL OBSERVATION; CONTROLLED STUDY; DENTIN; DNA DETERMINATION; DNA EXTRACTION; DNA SEQUENCE; EMBEDDING; EPIDEMIC; EUROPE; FRANCE; GENE AMPLIFICATION; HUMAN; HUMAN TISSUE; MEDICAL RESEARCH; NONHUMAN; PATHOGENESIS; PLAGUE; POLYMERASE CHAIN REACTION; POSTHUMOUS CARE; PRIORITY JOURNAL; SPECIES DIFFERENCE; TOOTH; VICTIM; YERSINIA PESTIS;

BACTERIA (MICROORGANISMS); NEGIBACTERIA; PROKARYOTA; YERSINIA; YERSINIA PESTIS;

EID: 1242273715     PISSN: 13500872     EISSN: None     Source Type: Journal    
DOI: 10.1099/mic.0.26594-0     Document Type: Article

References (74)

1. Aboudharam, G., La Scola, B., Raoult, D. & Drancourt, M. (2000). Detection of Coxiella burnetii in the dental pulp during experimental bacteremia. Microb Pathog 28, 249-254.
2. Austin, J. J., Ross, A. J., Smith, A. B., Fortey, R. A. & Thomas, R. H. (1997). Problems of reproducibility - does geologically ancient DNA survive in amber-preserved insects? Proc R Soc Lond B Biol Sci 264, 467-474.
3. Barnes, I., Matheus, P., Shapiro, B., Jensen, D. & Cooper, A. (2002). Dynamics of mammal population extinctions in Eastern Beringia during the last glaciation. Science 295, 2267-2270.
4. Basler, C. F., Reid, A. H., Dybing, J. K. & 9 other authors (2001). Sequence of the 1918 pandemic influenza virus nonstructural gene (NS) segment and characterization of recombinant viruses bearing the 1918 NS genes. Proc Natl Acad Sci U S A 98, 2746-2751.
5. Bate, A. L., Ma, J. K. & Pitt Ford, T. R. (2000). Detection of bacterial virulence genes associated with infective endocarditis in infected root canals. Int Endod J 33, 194-203.
6. Boom, R., Sol, C. J., Salimans, M. M., Jansen, C. L., Wertheim-van Dillen, P. M. & van der Noordaa, J. (1990). Rapid and simple method for purification of nucleic acids. J Clin Microbiol 28, 495-503.
7. Catranis, C. & Starmer, W. T. (1991). Microorganisms entrapped in glacial ice. Antarct J U S 26, 324-326.
8. Christner, B. C., Mosley-Thompson, E., Thompson, L. G., Zagorodnov, V., Sandman, K. & Reeve, J. N. (2000). Recovery and identification of viable bacteria immured in glacial ice. Icarus 144, 479-485.
9. Cohn, S. (2002). The Black Death Transformed: Disease and Culture in Early Renaissance Europe. London: Arnold.
10. Conrads, G., Gharbia, S. E., Gulabivala, K., Lampert, F. & Shah, H. N. (1997). The use of a 16S rDNA directed PCR for the detection of endodontopathogenic bacteria. J Endod 23, 433-438.
11. Cooper, A. (1994). DNA from museum specimens. In Ancient DNA, pp. 149-165. Edited by B. Hermann & S. Hummel. New York: Springer-Verlag.
12. Cooper, A. (1997). Reply to Stoneking: ancient DNA - how do you really known when you have it? Am J Hum Genet 60, 1001-1002.
13. Cooper, A. & Poinar, H. N. (2000). Ancient DNA: do it right or not at all. Science 289, 1139.
14. Cooper, A., Lalueza-Fox, C., Anderson, S., Rambaut, A., Austin, J. & Ward, R. (2001). Complete mitochondrial genome of two extinct moas clarify ratite evolution. Nature 409, 704-707.
15. Deng, W., Burland, V., Plunkett, G., 3rd & 18 other authors (2002). Genome sequence of Yersinia pestis KIM. J Bacteriol 184, 4601-4611.
16. Drancourt, M. & Raoult, D. (2002). Molecular insights into the history of plague. Microbes Infect 4, 105-109.
17. Drancourt, M., Aboudharam, G., Signoli, M., Dutour, O. & Raoult, D. (1998). Detection of 400-year-old Yersinia pestis DNA in human dental pulp: an approach to the diagnosis of ancient septicemia. Proc Natl Acad Sci U S A 95, 12637-12640.
18. Endicott, P., Gilbert, M. T., Stringer, C., Lalueza-Fox, C., Willerslev, E., Hansen, A. J. & Cooper, A. (2003). The genetic origins of the Andaman Islanders. Am J Hum Genet 72, 178-184.
19. Essack, S. Y., Hall, L. M., Pillay, D. G., McFayden, M. L. & Livermore, D. M. (2001). Complexity and diversity of Klebsiella pneumoniae strains with extended-spectrum beta-lactamases isolated in 1994 and 1996 at a teaching hospital in Durban, South Africa. Antimicrob Agents Chemother 45, 88-95.
20. Filippov, A. A., Solodovnikov, N. S., Kookleva, L. M. & Protsenko, O. A. (1990). Plasmid content in Yersinia pestis strains of different origin. FEMS Microbiol Lett 55, 45-48.
21. Finlay, B. J. & Clarke, K. J. (1999). Ubiquitous dispersal of microbial species. Nature 400, 828.
22. Finlay, B. J., Esteban, G. F., Olmo, J. L. & Tyler, P. A. (1999). Global distribution of free-living microbial species. Ecography 22, 138-144.
23. Fletcher, H. A., Donoghue, H. D., Holton, J., Pap, I. & Spigelman, M. (2003a). Widespread occurrence of Mycobacterium tuberculosis DNA from 18th-19th century Hungarians. Am J Phys Anthropol 120, 144-152.
24. Fletcher, H. A., Donoghue, H. D., Taylor, G. M., van der Zanden, A. G. & Spigelman, M. (2003b). Molecular analysis of Mycobacterium tuberculosis DNA from a family of 18th century Hungarians. Microbiology 149, 143-151.
25. Gilbert, M. T. P., Hansen, A. J., Willerslev, E., Rudbeck, L., Barnes, I., Lynnerup, N. & Cooper, A. (2003a). Characterisation of genetic miscoding lesions caused by post mortem damage. Am J Hum Genet 72, 48-61.
26. Gilbert, M. T. P., Willerslev, E., Hansen, A. J., Rudbeck, L., Barnes, I., Lynnerup, N. & Cooper, A. (2003b). Distribution patterns of post mortem damage in human mitochondrial DNA. Am J Hunt Genet 72, 32-47.
27. Graur, D. & Pupko, T. (2001). The Permian bacterium that isn't. Mol Biol Evol 18, 1143-1146.
28. Greer, C. E., Peterson, S. L., Kiviat, N. B. & Manos, M. M. (1991). PCR amplification from paraffin-embedded tissues. Effects of fixative and fixation time. Am J Clin Pathol 95, 117-124.
29. Gutierrez, G. & Marin, A. (1998). The most ancient DNA recovered from an amber-preserved specimen may not be as ancient as it seems. Mol Biol Evol 15, 926-929.
30. Haas, C. J., Zink, A., Molnar, E. & 7 other authors (2000). Molecular evidence for different stages of tuberculosis in ancient bone samples from Hungary. Am J Phys Anthropol 113, 293-304.
31. Handt, O., Hoss, M., Krings, M. & Paabo, S. (1994). Ancient DNA: methodological challenges. Experientia 50, 524-529.
32. Handt, O., Krings, M., Ward, R. & Pääbo, S. (1996). The retrieval of ancient human DNA sequences. Am J Hum Genet 59, 368-376.
33. Hansen, A., Willerslev, E., Wiuf, C., Mourier, T. & Arctander, P. (2001). Statistical evidence for miscoding lesions in ancient DNA templates. Mol Biol Evol 18, 262-265.
34. Hawkins, D. (1990). The Black Death and the new London cemeteries of 1348. Antiquity 60, 637-642.
35. Hinnebusch, J. & Schwan, T. G. (1993). New method for plague surveillance using polymerase chain reaction to detect Yersinia pestis in fleas. J Clin Microbiol 31, 1511-1514.
36. Hofreiter, M., Serre, D., Poinar, H. N., Kuch, M. & Pääbo, S. (2001). Ancient DNA. Nat Rev Genet 2, 353-359.
37. Hoshino, E., Naomi, A., Michiko, S. & Kohichi, K. (1992). Bacterial invasion of non-exposed dental pulp. Int Endod 125, 2-5.
38. Höss, M., Jaruga, P., Zastawny, T. H., Dizdaroglu, M. & Pääbo, S. (1996). DNA damage and DNA sequence retrieval from ancient tissues. Nucleic Acids Res 24, 1304-1307.
39. Khan, A. S., Sanchez, A. & Pflieger, A. K. (1998). Filoviral haemorrhagic fevers. Br Med Bull 54, 675-692.
40. Kiple, K. F. (1993). The Cambridge World History of Human Disease. Cambridge: Cambridge University Press.
41. Kolman, C. J. (1999). Molecular anthropology - progress and perspectives on ancient DNA technology. In Genomic Diversity: Applications in Human Population Genetics. Edited by S. S. Papiha & R. Deka. New York: Academic/Plenum Publishers.
42. Kolman, C. J. & Tuross, N. (2000). Ancient DNA analysis of human populations. Am J Phys Anthropol 111, 5-23.
43. Lynnerup, N. (1992). Anthropological Report on Human Remains from Vodroffsgaard, Copenhagen, AS 3/92. On file at the Laboratory of Biological Anthropology, University of Copenhagen, Copenhagen, Denmark.
44. Ma, L.-J., Rogers, S. O., Catranis, C. M. & Starmer, W. T. (1999). Detection and characterization of ancient fungi entrapped in glacial ice. Mycologia 92, 286-295.
45. Nerlich, A. G., Haas, C. J., Zink, A., Szeimies, U. & Hagedorn, H. G. (1997). Molecular evidence for tuberculosis in an ancient Egyptian mummy. Lancet 350, 1404.
46. Nickle, D. C., Learn, G. H., Rain, M. W., Mullins, J. I. & Mittler, J. E. (2002). Curiously modern DNA from a "250 million-year-old" bacterium. J Mol Evol 54, 134-137.
47. Nielsen-Marsh, C. & Hedges, R. E. M. (2000). Patterns of diagenesis in bone I: effects of site environments. J Archaeol Sci 27, 1139-1150.
48. Oota, H., Saitou, N., Matsushita, T. & Ueda, S. (1995). A genetic study of 2,000-year-old human remains from Japan using mitochondrial DNA sequences. Am J Phys Anthropol 98, 133-145.
49. Pääbo, S. (1989). Ancient DNA: extraction, characterization, molecular cloning, and enzymatic amplification. Proc Natl Acad Sci U S A 86, 1939-1943.
50. Parkhill, J., Wren, B. W., Thomson, N. R. & 32 other authors (2001). Genome sequence of Yersinia pestis, the causative agent of plague. Nature 413, 523-527.
51. Pfeiffer, H., Huhne, J., Seitz, B. & Brinkmann, B. (1999). Influence of soil storage and exposure period on DNA recovery from teeth. Int J Legal Med 112, 142-144.
52. Rafi, A., Spigelman, M., Stanford, J., Lemma, E., Donoghue, H. & Zias, J. (1994). Mycobacterium leprae DNA from ancient bone detected by PCR. Lancet 343, 1360-1361.
53. Raoult, D. & Drancourt, M. (2002). Cause of Black Death. Lancet Infect Dis 2, 459.
54. Raoult, D., Aboudharam, G., Crubezy, E., Larrouy, G., Ludes, B. & Drancourt, M. (2000). Molecular identification by "suicide PCR" of Yersinia pestis as the agent of medieval black death. Proc Natl Acad Sci U S A 97, 12800-12803.
55. Reid, A. H., Fanning, T. G., Hultin, J. V. & Taubenberger, J. K. (1999). Origin and evolution of the 1918 "Spanish" influenza virus hemagglutinin gene. Proc Natl Acad Sci U S A 96, 1651-1656.
56. Richards, M., Sykes, B. & Hedges, R. (1995). Authenticating DNA extracted from ancient skeletal remains. J Archaeol Sci 22, 291-299.
57. Ringboel Bitsch, B. (1991). Archaeological Excavation Report "Vodroffsgaard", KBM 836. On file at Copenhagen City Museum, Copenhagen, Denmark.
58. Rothschild, B. M., Martin, L. D., Lev, G., Bercovier, H., Bar-Gal, G. K., Greenblatt, C., Donoghue, H., Spigelman, M. & Brittain, D. (2001). Mycobacterium tuberculosis complex DNA from an extinct bison dated 17,000 years before the present. Clin Infect Dis 33, 305-311.
59. Salo, W. L., Aufderheide, A. C., Buikstra, J. & Holcomb, T. A. (1994). Identification of Mycobacterium tuberculosis DNA in a pre-Columbian Peruvian mummy. Proc Natl Acad Sci U S A 91, 2091-2094.
60. Scott, S. & Duncan, C. (2001). Biology of Plagues: Evidence from Historical Populations. Cambridge: Cambridge University Press.
61. Shapiro, B., Sibthorpe, D., Rambaut, A., Austin, J., Wragg, G. M., Bininda-Emonds, O. R. P., Lee, P. L. M. & Cooper, A. (2002). Flight of the dodo. Science 295, 1683.
62. Spigelman, M., Matheson, C., Lev, G., Greenblatt, C. & Donoghue, H. (2002). Confirmation of the presence of Mycobacterium tuberculosis complex-specific DNA in three archaeological specimens. Int J Osteoarch 12, 393-401.
63. Stephens, J. C., Reich, D. E., Goldstein, D. B. & 36 other authors, (1998). Dating the origin of the CCR5-Delta32 AIDS-resistance allele by the coalescence of haplotypes. Am J Hum Genet 62, 1507-1515.
64. Taubenberger, J. K., Reid, A. H., Krafft, A. E., Bijwaard, K. E. & Fanning, T. G. (1997). Initial genetic characterization of the 1918 "Spanish" influenza virus. Science 275, 1793-1796.
65. Taylor, G., Crossey, M., Saldanha, J. & Waldron, T. (1996). DNA from Mycobacterium tuberculosis identified in medieval human skeletal remains using PCR. J Archaeol Sci 23, 789-799.
66. Titball, R. W. & Williamson, E. D. (2001). Vaccination against bubonic and pneumonic plague. Vaccine 19, 4175-4184.
67. Von Kohl, C. (1911). Historiske Meddelelser om København. Copenhagen, 1911-12. GEC Gad 3, 545-614 (in Danish).
68. Vreeland, R. H., Rozenwieg, W. D. & Powers, D. W. (2000). Isolation of a 250 million-year-old halotolerant bacterium from a primary salt crystal. Nature 407, 897-900.
69. Waldron, H. (2001). Are plague pits of particular use to palaeoepidemiologists? Int J Epidemiol 30, 104-108.
70. Willerslev, E., Hansen, A. J., Christensen, B., Steffensen, J. P. & Arctander, A. (1999). Diversity of Holocene life forms in fossil glacier ice. Proc Natl Acad Sci U S A 96, 8017-8021.
71. WHO. (1999). Plague Manual: Epidemiology, Distribution, Surveillance and Control (http://www.who.int/csr/resources/publications/plague/ WHO_CDS_CSR_EDC_99_2_EN/en). Geneva: World Health Organization.
72. Yersin, A. (1894). La peste bubonique à Hong Kong. Ann Inst Pasteur (Paris) 8, 662-667.
73. Zhang, L., Cui, A., Schmitt, K., Hubert, R., Navidi, W. & Amheim, N. (1992). Whole genome amplification from a single cell: implications for genetic analysis. Proc Natl Acad Sci U S A 89, 5847-5851.
74. Zink, A., Haas, C. J., Reischl, U., Szeimies, U. & Nerlich, A. G. (2001). Molecular analysis of skeletal tuberculosis in an ancient Egyptian population. J Med Microbiol 50, 355-366.