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The existence of Mycobacterium tuberculosis in the Americas prior to European contact

The existence of Mycobacterium tuberculosis in the Americas prior to European contact. Steven Weger MMIC 7050 March 25 2013. Outline. Background Information Detection in Ancient Samples Origin of TB Prehistoric Findings: South America Prehistoric Findings: North America Future Directions

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The existence of Mycobacterium tuberculosis in the Americas prior to European contact

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  1. The existence of Mycobacterium tuberculosis in the Americas prior to European contact Steven Weger MMIC 7050 March 25 2013

  2. Outline • Background Information • Detection in Ancient Samples • Origin of TB • Prehistoric Findings: South America • Prehistoric Findings: North America • Future Directions • Conclusion

  3. Tuberculosis • Tubercle = Bacteria-containing lesions • Bacteria are taken up by macrophage and reside inside cell • “Disease of Poverty” (http://bepast.org/dataman.pl?c=flib&dir=docs/photos/MDR%20tuberculosis/)

  4. Tuberculosis • One of the leading causes of death worldwide • 1.4 million die each year • 90% of infections develop into latent TB • No symptoms, not contagious • Many people with latent form never develop active infection http://bepast.org/dataman.pl?c=flib&dir=docs/photos/MDR%20tuberculosis/

  5. Tuberculosis • Activation: immune system is weakened • Old age, malnutrition, pregnancy, HIV, diabetes • Developing world: infects 1/3 of people • Causes tissue destruction, leading to rupturing of blood vessels and hemorrhaging • Symptoms: • Begins with bad cough that produces blood-tinged phlegm and lasts for 3 weeks or more • chest pain, fatigue, loss of appetite, weight loss, fever, chills and night sweating

  6. Tuberculosis • Mycobacterium tuberculosis complex (MTBC) • Most commonly caused by Mycobacterium tuberculosis • Also M. africanum, M. canetti, M. bovis, M. microti, M. pinnipedii, M. caprae • Genetically very closely related • Different host ranges and pathogenicities

  7. History • Bacteria emerged over 70,000 years ago • Co-existed with humans for 40,000 years • Paleopathological: from 5380-4940 calBC in Germany • Historical: 2700 BC in China • Rise in prevalence due to increases in population density http://news.discovery.com/human/health/tb-has-ancient-history-130905.htm

  8. Identifying Ancient TB • Skeleton is altered in 3-5% of TB cases • Can affect any bone • 25-50% of untreated patients develop spinal changes • Lead to kyphosis-> Pott’s disease • Non-specific lesions: skulls ribs, new bone formation on long bones, dactylitis, calcified pleura http://www.livescience.com/2871-skeleton-early-tb-victim.html

  9. Detecting Ancient TB • PCR • TB is first infectious disease to be detected in bones and mummified tissue • Based on MTBC-specific locus IS6110 • Present in multiple copies per cell

  10. Detecting Ancient TB • High-performance liquid chromatography (HPLC) • MTBC-specific mycolic acid • No amplification step-> no false-positives • Mass spectrometry • Dimycocerosic acid http://en.wikipedia.org/wiki/File:Hplc.JPG

  11. Origin of TB in Americas • 2 major American migrations -> 25,000 years ago and 10,000 years ago • Mycobacterial DNA identified in a pulmonary lesion of a 10000-year-old Peruvian mummy • 1st molecular diagnosis of TB • Earliest evidence of TB in the Americas come from Peruvian mummies of the first millennium http://www.amusingplanet.com/2010/07/mummies-of-world.html

  12. Origin of Human Tuberculosis • M. tuberculosis or M. bovis? • Traditional hypothesis: M. bovis contact initiated during domestication of the aurochs (cattle) during the Neolithic revolution • Contaminated milk and beef • Evolution of sedentary settlements favored selection of the respiratory form, caused by M. tuberculosis http://schaechter.asmblog.org/.a/6a00d8341c5e1453ef01676755890b970b-popup

  13. Origin of Human Tuberculosis • Typical crowd disease • Kills up to 50% of those infected if untreated • Aerosol transmission mode promotes spread of disease in high population densities • TB --> Chronic, long-duration disease • Possible that M. tuberculosis persisted at low endemic levels even in small populations http://bepast.org/dataman.pl?c=flib&dir=docs/photos/MDR%20tuberculosis/

  14. Native Americans and TB • Was TB present before European contact? • Terrible outbursts suggest low immunity • “Virgin soil” • However, paleopathological studies confirmed presence of disease in different prehistoric American populations

  15. Prehistoric Findings: S. America TB persisted in S. America for over 2000 years, most ancient case  160 BC • Mackowiak PA, Blos VT, Aguilar M, Buikstra JE. On the Origin of American Tuberculosis. Clininf dis 2005; 41:515-8. 

  16. Prehistoric Findings: N. America • Mackowiak PA, Blos VT, Aguilar M, Buikstra JE. On the Origin of American Tuberculosis. Clininf dis 2005; 41:515-8.  • More uniform Record • TB was endemic for the Pueblos • Long chronological cultural sequence 150BC-1150 AD • None of these cases confirmed molecularly

  17. Future Studies • Molecular based approaches • Whole genome sequence analysis • Compare ancient vs modern lineages • Follow evolution of TB and co-evolution with humans • Determine cause of prehistoric TB in Americas • M. bovisvsM. tuberculosis debate

  18. Biomolecular Identification of Ancient Mycobacterium tuberculosis Complex DNA in Human Remains From Britain and Continental Europe -Brown et al. -American Journal of Physical Anthropology -2014

  19. Materials and Methods • Skeletons collected from British and other European sites • Wore forensic suits, hairnets, facemasks, and sterile gloves • Samples stored under dry conditions in plastic bags • aDNA extractions and PCRs carried out in physically isolated independent laboratories • Manchester, England • Madrid, Spain • Modern MTBC DNA was not present in building

  20. Materials and Methods • Outer 1-2mm surface of bones removed remaining sample UV irradiated • Two DNA extractions performed • Protocol 1 (Bouwman and Brown) • Protocol 2 (Rohland and Hofreiter) • qPCR • Directed at 63 bp sequence of IS1081 • PCR • 123 bp segment of IS6110 • Nested PCR • On samples that did not produce the 123 bp product • PCR products of correct size were cloned into E. coli • Sequenced and aligned w/ M. tuberculosis H37Rv reference sequence for IS6110

  21. Results of the Molecular Analysis • Muller R, Roberts CA, Brown TA. Biomlecular Identification of Ancient Mycobacterium tuberculosis Complex DNA in Human Remains From Britain and Continental Europe. American Journal of Physical Anthropology 2014; 153:178-189.

  22. Association of Pathological Lesionsw/ MTBC aDNA Detection • Muller R, Roberts CA, Brown TA. Biomlecular Identification of Ancient Mycobacterium tuberculosis Complex DNA in Human Remains From Britain and Continental Europe. American Journal of Physical Anthropology 2014; 153:178-189.

  23. Conclusion • Archaeological proves TB has already been present in America for at least 2,000 years before contact by Europeans • TB had already developed an epidemiological pattern of aerial transmission • Paleopathologicalinformation is still insufficient for a complete epidemiological reconstruction of tuberculosis in America • MTBC most likely came to the Americas with the first human migrants • More molecular studies must be conducted to further investigate origin of MTBC in Americas

  24. References • WHO (World Health Organization). Global tuberculosis report 2012. Geneva: World Health Organization 2012. • Muller R, Roberts CA, Brown TA. Biomlecular Identification of Ancient Mycobacterium tuberculosis Complex DNA in Human Remains From Britain and Continental Europe. American Journal of Physical Anthropology 2014; 153:178-189. • Vincent V, Gutierrez Perez MC. The agent of tuberculosis. Budapest: Golden Book Publisher 1999; 139–143. • Gutierrez M, Samper S, Jimenez MS, van Embden JDA, Marin JF, Martin C. Identification by spoligotyping of a caprine genotype in Mycobacterium bovis strains causing human tuberculosis. J ClinMicrobiol 1997; 35:3328–3330. • Tsukamura M, Mizuno S, Toyama H. Taxonomic studies on the Mycobacterium tuberculosis series. MicrobiolImmunol 1985; 29285-29299. • Feizabadi M, Robertson ID, Cousins DV, Hampson DJ. Genomic analysis of Mycobacferiumbovis and other members of the Mycobacterium tuberculosis complex by isoenzyme analysis and pulsed-field gel electrophoresis. J ClinMicrobiol 1996; 341136-1142. • van Soolingen D, Hermans PWM, de Haas PEW, Soll DR, van Embden JDA. The occurrence and stability of insertion sequences in Mycobacterium tuberculosis complex strains: evaluation of an insertion sequence-dependent DNA polymorphism as a tool in the epidemiology of tuberculosis. J ClinMicrobiol 1991; 292578-2586. • Wayne LG, Kubica GP. The mycobacteria. Bergey’s manual of systematic bacteriology 1986; 2:1435-1457. • Comas I, Coscolla M, Luo T, Borrell S, Holt KE, Kato-Maeda M, Parkhill J, Malla B, Berg S, Thwaites G, Yeboah-Manu D, Bothamley G, Mei J, Wei L, Bentley S, Harris SR, Niemann S, Diel R, Aseffa A, Gao Q, Young D, Gagneux S. Out-of-Africa migration and Neolithic coexpansion of Mycobacterium tuberculosis with modern humans. Nat Genet 2013; 45:1176– 1182. • Nicklisch N, Maixner F, Ganslmeier R, Friederich S, Dresely V, Meller H, Zink A, Alt KW. Rib lesions in skeletons from Early Neolithic sites in Central Germany: on the trail of tuberculosis at the onset of agriculture. Am J PhysAnthropol2012; 149:391–404. • Morse D. Tuberculosis. Springfield: Charles Thomas 1967; 249–271. • Roberts CA, Buikstra JE. The bioarchaeology of tuberculosis. A global view on a re-emerging disease. Gainesville: University Press of Florida 2003. • Resnick D. Diagnosis of bone and joint disorders. Philadelphia: W.B. Saunders 2002; 3(4):4844–4919. • Schultz M. The role of tuberculosis in infancy and childhood in prehistoric and historic populations. Budapest: Golden Book Publisher 1999; 503–507. • Tatelman M, Drouillard EJP. Tuberculosis of the ribs. Am J Roentgenol 1953. 70:923–935. • Spigelman M, Lemma E. The use of the polymerase chain reaction (PCR) to detect Mycobacterium tuberculosis in ancient skeletons. Int J Osteoarchaeol 1993; 3:137–143. • Zink AR, Haas CJ, Reischl U, Szeimies U, Nerlich AG. Molecular analysis of skeletal tuberculosis in an ancient Egyptian population. J Med Microbiol 2001; 50:355–366. • Redman JE, Shaw MJ, Mallet AI et al. Mycocerosic acid biomarkers for the diagnosis of tuberculosis in the Coimbra skeletal collection. Tuberculosis (Edinb) 2009; 89:267–277. • Salo W, Aufderheide A C, Buikstra J, Holcomb TA. Identification of Mycobacterium tuberculosis DNA in a pre-Columbian Peruvian mummy. ProcNatlAcadSci USA 1994; 91:2091–2094. • Nowak RM. Walker’s Mammals of the World. John Hopkins University Press, Baltmore 1991; 1425-1431. • Cockburn A. Infectious Diseases: Their Evolution and Erradication. Charles C Thomas, Springfield 1967; 402. • Comas I, Coscolla M, Luo T, Borrell S, Holt K, Kato-Maeda M, Parkhill J, Malla B, Berg S, Thwaites G, Yeboah-Manu D, Bothamley G et al. Out-of-Africa migration and Neolithic coexpansion of Mycobacterium tuberculosis with modern humans. Nature Genetics 2013; 45(10):1176-1182. • Kiple KF. The Cambridge World History of Human Disease. Cambridge University Press, New York, 2012; 1059-1068. • Allison M, Gerszten E, Munizaga J, Santoro C, Mendoza D. Tuberculosis in pre-Columbian andean populations. Northwestern University Archaeological Program, Evanston, 1981; 49-61. • Prat JG, Souza S. Prehistoric Tuberculosis in America: Adding Comments to a Literature Review. MemInstOswaldo Cruz, Rio de Janeir2003; 98:151-159. • Sumner DR. A probable case of Prehistoric tuberculosis from northeastern Arizona. Arizona State University, Anthropological Research Papers 1985; 34. • Buikstra JE. Prehistoric Tuberculosis in the Americas. Northwestern University Archaelogical Program, Evanston, 1981; 182. • Mackowiak PA, Blos VT, Aguilar M, Buikstra JE. On the Origin of American Tuberculosis. Clininf dis 2005; 41:515-8.

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