Mycolic Acids as Markers of Osseous Tuberculosis in the Neolithic Skeleton from Kujawy Region (Central Poland)
DOI:
https://doi.org/10.2478/anre-2014-0012Keywords:
mycolic acids, paleopathology,, NeolithicAbstract
The subject of analysis is the male skeleton from a double burial of the Globular Amphora Culture, derived from the Neolithic site at Brześć Kujawski in Kujawy region (central Poland). Within the spine of the individual advanced lesions are observed (destruction of the vertebral bodies, symptoms of the periostitis in the thoracic region) which are characteristic of skeletal tuberculosis. To check whether the observed morphological changes resulted from infection with Mycobacterium tuberculosis (M.tb), the bone material was tested positively for the presence of mycolic acids, the specific components of the cell wall of pathogenic M.tb bacilli, by mass spectrometry.
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References
Aufderheide AC, Rodríguez-Martín C. 1998. The Cambridge Encyclopedia of Human Paleopathology. Cambridge: Cambridge University Press.
View in Google Scholar
Bartels P. 1907. Tuberkulose in der Jungeren Steinzeit. Archiv für Anthropologie 6:243–55.
View in Google Scholar
Bouwman AS, Kennedy SL, Müller R, Stephens RH, Holst M, Caffell AC, Roberts ChA, Brown TA. 2012. Genotype of a historic strain of Mycobacterium tuberculosis. Proc Natl Acad Sci 109(45):18511–16.
View in Google Scholar
Brosch R, Gordon SV, Marmiesse M, Brodin P, Buchrieser C, Eiglmeier K, et al. 2002. A new evolutionary scenario for the Mycobacterium tuberculosis complex. Proc Natl Acad Sci 99(6):3684–89.
View in Google Scholar
Brothwell DR. 1981. Digging Up Bones: The Excavation, Treatment, and Study of Human Skeletal Remains. Cornell University Press.
View in Google Scholar
Canci A, Minozzi S, Borgognini Tarli SM. 1996. New evidence of tuberculous spondylitis from Neolithic Liguria (Italy). Int J Osteoarchaeol 6:497–501.
View in Google Scholar
Chan JZ-M, Sergeant MJ, Lee OY-C, Minnikin DE, Besra GS, et al. 2013. Metagenomic analysis of tuberculosis in a mummy. N Engl J Med 369:289–90.
View in Google Scholar
Donoghue HD, Spigelman M, Greenblatt CL, Lev-Maor G, Bar-Gal GK, et al. 2004. Tuberculosis: from prehistory to Robert Koch, as revealed by ancient DNA. Lancet Infectious Diseases 4:584–92. doi: 10.1002/cne.900340202
View in Google Scholar
El-Najjar M, Al-Shiyab A, Al-Sarie I. 1997. Cases of tuberculosis at ‘Ain Ghazal, Jordan. Paléorient 22(2):123–28.
View in Google Scholar
Fijałek A, Supady J. 2002. Pulmonary tuberculosis in Lodz since the late nineteenth century to 1918 r.: on the history of the fight against disease, ADI Lodz.
View in Google Scholar
Formicola V, Milanesi Q, Scarsini C. 1987. Evidence of spinal tuberculosis at the beginning of the fourth millennium BC from Arene Candide cave (Liguria, Italy). Am J Phys Anthropol 72:1–6.
View in Google Scholar
Gernaey AM, Minnikin DE, Copley MS, Ahmed AMS, Robertson DJ, et al. 1999. Correlation of the occurrence of mycolic acids with tuberculosis in an archaeological population. In: Pálfi G, Dutour O, Deák J, Hutás I, editors. Tuberculosis, Past and Present: Golden Book Publisher Ltd., Tuberculosis Foundation. 275–82.
View in Google Scholar
Gernaey AM, Minnikin DE, Copley MS, Dixon RA, Middleton JC, et al. 2001. Mycolic acids and ancient DNA confirm an osteological diagnosis of tuberculosis. Tuberculosis 81:259–65. doi: 10.1054/tube.2001.0295.
View in Google Scholar
Gładykowska-Rzeczycka JJ. 2008. Paleoepidemia – archeoepidemie [in:] Dzieduszycki W, Wrzesiński J (eds), Epidemie, klęski, wojny. Funeralia Lednickie – spotkanie 10, Poznań:37–52.
View in Google Scholar
Golden MP, Vikram HR. 2005. Extrapulmonary tuberculosis: an overview. Am Fam Physician 72(9):1761–68.
View in Google Scholar
Hershkovitz I, Donoghue HD, Minnikin DE, Besra GS, Lee OY-C, et al. 2008. Detection and Molecular Characterization of 9000-Year-Old Mycobacterium tuberculosis from a Neolithic Settlement in the Eastern Mediterranean. PLoS One 3:e3426.
View in Google Scholar
Holloway KL, Henneberg RJ, de Barros Lopes M, Henneberg M. 2011. Evolution of human tuberculosis: A systematic review and meta-analysis of paleopathological evidence. HOMO 62(6):402–58.
View in Google Scholar
Jażdżewski K. 1938. Cmentarzyska kultury wstęgowej i związane z nimi ślady osadnictwa w Brześciu Kujawskim. Wiad Archeol 15:1–105.
View in Google Scholar
Laval F, Lanéelle MA, Déon C, Monsarrat B, Daffé M. 2001. Accurate molecular mass determination of mycolic acids by MALDI-TOF mass spectrometry. Anal Chem 73(18): 4537–44.
View in Google Scholar
Lee OY-C, Bull ID, Molnár E, Marcsik A, Pálfi G, Donoghue HD, Besra GS, Minnikin DE. 2012. Integrated strategies for the use of lipid biomarkers in the diagnosis of ancient mycobacterial disease. In: PD Mitchell and J Buckberry, editors. Proceedings of the 12th Annual Conference of the British Association for Biological Anthropology and Osteoarchaeology. UK, Oxford: Archaeopress. 63–69.
View in Google Scholar
Masson M, Molnár E, Donoghue HD, Besra GS, Minnikin DE,Wu H-HT, Lee OY-C, Bull IE, Pálfi G. 2013. Osteological and Biomolecular Evidence of a 7000-Year-Old Case of Hypertrophic Pulmonary Osteopathy Secondary to Tuberculosis from Neolithic Hungary, PLoS One 8:10. doi: 10.1371/journal.pone.0078252.
View in Google Scholar
Minnikin DE, Lee OY-C, Wu H-HT, Besra GS, Donoghue HD. 2012. Molecular Biomarkers for Ancient Tuberculosis. In: PJ Cardona, editor. Understanding Tuberculosis – Deciphering the Secret Life of the Bacilli. Rijeka, Croatia: InTech – Open Access Publisher. 1–36.
View in Google Scholar
Müller R, Roberts C, Brown TA. 2013. Biomolecular identification of ancient Mycobacterium tuberculosis complex DNA in human remains from Britain and continetal Europe. Am J Phys Anthropol. doi: 10.1002/ajpa.22417.
View in Google Scholar
Ortner DJ. 2003. Identifications of Pathological Conditions in Human Skeletal Remains. San Diego: Academic Press, Elsevier Science.
View in Google Scholar
Redman JE, Shaw MJ, Mallet AI, Santos AL, Roberts C, et al., 2009. Mycocerosic acid biomarkers for the diagnosis of tuberculosis in the Coimbra Skeletal Collection. Tuberculosis 89:267–77.
View in Google Scholar
Resnick D. (ed.) 1995. Diagnosis of bone and joint disorders. Edinburgh: W.B. Saunders.
View in Google Scholar
Roberts CA, Lucy D, Manchester K. 1994. Inflammatory lesions of ribs: an analysis of the Terry Collection. Am J Phys Anthropol 95:169–82.
View in Google Scholar
Roberts CA, Buikstra JE. 2003. The Bioarchaeology of Tuberculosis: A Global View on a Reemerging Disease. University Press of Florida.
View in Google Scholar
Sager P., Schalimtzek M., Möller-Christensen V. 1972. A case of spondylitis tuberculosa in the Danish Neolithic age. Danish Medical Bulletin 19:176–80.
View in Google Scholar
Sajduda A, Brzostek A, Popławska M, Augustynowicz-Kopeć E, Zwolska Z, Niemann S, Dziadek J, Hillemann D. 2004. Molecular characterization of rifampin- and isoniazid-resistant Mycobacterium tuberculosis strains isolated in Poland. J Clin Microbiol 42(6):2425–31.
View in Google Scholar
Shui G, Bendt AK, Pethe K, Dick T, Wenk MR. 2007. Sensitive profiling of chemically diverse bioactive lipids. J Lipid Res 48:1976–84.
View in Google Scholar
Shui G, Bendt AK, Jappar IA, Lim HM, Laneelle M, Herve M, Via LE, Chua GH, Bratschi MW, Rahim SZZ, Michelle ALT, Hwang S-H, Lee J-S, Eum S-Y, Kwak HK, Daffe M, Dartois V, Michel G, Barry CE III, Wenk MR. 2012. Mycolic acids as diagnostic markers for tuberculosis detection in humans and drug efficacy in mice. EMBO Mol Med 4(1):27–37.
View in Google Scholar
Song SH, Park KU, Lee JH, Kim EC, Kim JQ, Song J.2009. Electrospray ionization-tandem mass spectrometry analysis of the mycolic acid profiles for the identification of common clinical isolates of mycobacterial species. J Microbiol Methods 77(2):165–77.
View in Google Scholar
Szewczyk R, Kowalski K, Janiszewska-Drobinska B, Druszczyńska M. 2013. Rapid method for Mycobacterium tuberculosis identification using electrospray ionization tandem mass spectrometry analysis of mycolic acids. Diagn Microbiol Infect Dis 76:298–305.
View in Google Scholar
Takayama K, Wang C, Besra GS. 2005. Pathway to synthesis and processing of mycolic acids in Mycobacterium tuberculosis. Clin Microbiol Rev 18(1):81–101.
View in Google Scholar
Tran T-NN, Aboudharam G, Raoult D, Drancourt M. 2011. Beyond ancient microbial DNA: nonnucleotidic biomolecules for paleomicrobiology. BioTechniques 50(6):370–80.
View in Google Scholar
Watanabe M, Aoyagi Y, Mitome H, Fujita T, Naoki H, Ridell M, Minnikin DE. 2002. Location of functional groups in mycobacterial meromycolate chains; the recognition of New structural principles in mycolic acids. Microbiology 148:1881–902.
View in Google Scholar
White TD, Folkens PA. 2005. The Human Bone Manual, Academic Press.
View in Google Scholar
World Health Organisation, Global Tuberculosis Report. 2013 http://www.who.int/tb/publications/global_report/en/
View in Google Scholar
Zink AR, Molnár E, Motamedi N, Pálfi G, Marcsik A, et al. 2007. Molecular History of Tuberculosis from Ancient Mummies and Skeletons. Int J Osteoarchaeol 17:380–91.
View in Google Scholar
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