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Durham University

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Biomolecular archaeology of ancient tuberculosis in Britain and Europe

A research project of the Department of Archaeology.

Background

This Natural Environmental Research Council funded project ran from 2007 to 2011 and was headed by Professor Roberts (£173,825 to Durham) and Professor Terry Brown (Life Sciences, University of Manchester); completing the research team were Dr Abigail Bouwman (Postdoctoral Research Assistant, based at Manchester), Dr Darlene Weston (Research Associate, based at Durham), and a linked research student (Kirsty McCarrison). It expanded research already completed on the bioarchaeology of tuberculosis by Professor Roberts (see references below).

Tuberculosis (TB), a re-emerging infectious disease, infects ⅓ of the world's population today, and was responsible for 1.7 million deaths in 2004. It is the culmination of a global history probably extending over 3 million years in the Old World, originating in Africa. Among the causative factors in the increase in TB are HIV/AIDS, poverty, antibiotic resistance, travel, and migration. In the past poverty, movement of people, and contact with infected animals were probably the main environmental variables that enabled TB to develop. The Mycobacterium tuberculosis complex mainly describes the organisms which can cause TB in humans. M. tuberculosis and M. bovis cause TB in mammals, M. africanum in humans in some African countries, and M. microti in voles. Although not considered relevant for the origin/evolution of TB in Britain, the M. avium complex is also a source of TB in humans. Humans contract TB via droplet spread (coughing and sneezing) or through consuming infected meat and milk from animals and, if not treated, the infection spreads to the bone via the blood and lymphatic systems, changes in the spine most often being used for diagnosis in palaeopathology. However, only 3-5% of people infected with TB display these skeletal indicators.

The first clear historical evidence for TB dates back to China at 2700 BC. The first skeletal evidence derives from Italy dated to 5800±90 BC, with the first evidence from the New World (South America) dating to AD 700. However, in Europe, it is not until the late- and post-Medieval periods that TB increases in frequency - in Britain the London Bills of Mortality indicate up to 25% of people died from the infection in the 1780s and 1790s. In Britain the first skeletal evidence (confirmed with ancient DNA analysis) is from the Iron Age (400-230 BC) at Tarrant Hinton, Dorset, with further people infected in the Roman period, mainly located (i.e. buried) in the southern half of England, especially in Dorset, Gloucestershire and Northamptonshire. Despite its long history, however, TB has not reduced in virulence to a state of benign commensalism with humans. Indeed, although the development of antibiotic therapy in the 1940s brought about the hope of TB's eradication by the end of the century it became apparent that the disease was again on the rise, and it is now considered by the World Health Organisation to be a global emergency.

It is generally accepted that biomolecular archaeology, specifically the study of ancient DNA (aDNA), has enormous potential in the study of palaeopathology or the history of disease. Theoretically, any pathogen that invades the blood system and/or hard tissues of the body such as bone could leave an aDNA signature in skeletal remains after the death of the host. To date, most of the attention in biomolecular palaeopathology has been focused on TB, with a growing body of reliable literature describing the use of PCR (polymerase chain reaction) to amplify M. tuberculosis complex DNA from human bones of various ages. Many of the early studies (early 1990s) of M. tuberculosis complex DNA in human bones were aimed merely at confirming or extending the osteological indications for TB in a skeletons from archaeological sites but, as the field has matured, more informative strategies have been adopted. For example, SNP typing has been used to distinguish between three different lineages of M. tuberculosis complex in skeletons from a post-Medieval Hungarian cemetery, and spoligotyping has been used to differentiate M. tuberculosis strains in late Medieval skeletal remains in Britain. The RD regions - deletions that can be used to distinguish between species and strains of the M. tuberculosis complex - have also been typed in aDNA.

The project built on these previous studies. We aimed to study the origin and evolution of the causative agents of TB in Britain and other parts of Europe from analysing samples of bone from skeletons of different dates.

Progress on the project

The first year of the project was devoted to arranging access to, and the acquisition of samples from, skeletons with tuberculous changes curated in museums and other institutions in the UK and the rest of Europe. Dr Darlene Weston completed her year on the project as Research Associate and all (several hundred) samples were collected. Dr Abigail Bouwman then analysed all the samples at the University of Manchester. The initial screening for TB aDNA was completed and the analysis of bacterial subtypes followed; the project ended in 2011. The outputs from the project continue, but are detailed below.

Conference presentations

Annual Meeting of the American Association of Physical Anthropologists, Knoxville, Tennessee, USA 2013: Session on infectious disease in humans and other primates: Bouwman et al: Ancient tuberculosis DNA revealed by Next Generation Sequencing

British Association of Biological Anthropology and Osteoarchaeology Annual Conference, University of York, England 2013: R Müller et al: Identification of ancient Mycobacterium tuberculosis strains in human skeletal remains

Annual Meeting of the American Association of Physical Anthropologists, Portland, Oregon, USA 2012: Roberts et al: Understanding Re-emerging Infectious Diseases: Contributions on Tuberculosis from Palaeopathology and Biomolecular Science

ICEPT -2. The past and present of tuberculosis: a multidisciplinary overview of the origin and evolution of TB, Szeged, Hungary 2012: Roberts: Old World tuberculosis: evidence from human remains with a review of current research and future prospects; Müller et al: Tuberculosis across Europe – an ancient DNA study

Annual Meeting of the American Association of Physical Anthropologists, Minneapolis, Minnesota, USA 2011: Bouwman et al: An ancient DNA study of tuberculosis in Europe

BABAO Annual Meeting, University of Edinburgh: Roberts 2011: Understanding re-emerging infectious diseases: contributions on tuberculosis from palaeopathology and biomolecular science

18th Paleopathology Association European Meeting, Vienna, Austria 2010: Müller et al: Tuberculosis in Roman Britain: an ancient DNA approach; Bouwman et al: An ancient DNA survey of archaeological tuberculosis in Europe

Outreach

Edinburgh University Archaeology Society 2013 Interpreting the impact of infections on people using bioarchaeology: How palaeopathology can be used to answer questions about the past (Roberts)
British Science Festival, University of Newcastle 2013: Plague and Pestilence: Which was the Most Important Disease to Have Affected People in Britain in the Past? Panel discussion about leprosy, plague, syphilis and tuberculosis (Roberts on TB)
University of Pisa, Italy 2009 - The palaeopathology of tuberculosis: what we know, and how biomolecular techniques are helping us understand more about this reemerging infection (Roberts).
Northumberland Archaeology Group 2010 - Prehistoric TB in Britain? Bones and the secrets they hold (McCarrison)
Durham University Researchers' Poster Competition 2010: The Hunt for an Ancient Killer
University of Sheffield 2009 - Tuberculosis: can bioarchaeology help us understand this re-emerging infectious disease? (Roberts)
Researchers Revealed 2009 - a European Wide Public Engagement Event (coordinated by the European Commission). Discussed Project with Public (McCarrison).
Science Poster Showcase - The British Science Association sponsored Public Lecture 2009: The Hunt for an Ancient Killer (McCarrison)
UK Grad Poster Competition (Yorkshire and North East Hub) March 2008: Prehistoric Tuberculosis: An Archaeological Mystery (McCarrison)
University of Birmingham Medical School 2008: Ancient DNA Analysis (McCarrison)
Durham University Researchers' Poster Competition 2008: An Osteological and Biomolecular Study of Prehistoric Tuberculosis in Britain (McCarrison)

Publications

Bouwman AS, Kennedy SL, Muller R, Stephens RH, Holst M, Caffell AC, Roberts CA, Brown TA 2012 The genotype of a historic strain of Mycobacterium tuberculosis. Proc Natl Acad Sci USA 109: 18511–18516

Roberts CA 2012 Re-emerging infections: developments in bioarchaeological contributions to understanding tuberculosis today. In A Grauer (ed): A companion to paleopathology. Wiley-Blackwell, 434-457.

Assis S, Santos AL, Roberts CA. 2011. Evidence of hypertrophic osteoarthropathy in individuals from the Coimbra Skeletal Identified Collection (Portugal). Int J Palaeopathology 1:155-163

Roberts CA 2011 The bioarchaeology of leprosy and tuberculosis in late Medieval England: a comparative study of perceptions, stigma, diagnosis and treatment. In B Glencross and S Agarwal (eds): Handbook of Social Archaeology. Blackwell Studies in Global Archaeology. Chichester, Wiley Blackwell, pp. 252-281

Stone AC, Wilbur AK, Buikstra JE & Roberts CA. 2009. Mycobacterial disease in perspective. American Journal of Physical Anthropology 140(Yearbook 49): 66-94.

Redman JE, Shaw MJ, Mallet AI, Santos AL, Roberts CA, Gernaey AM & Minnikin DE. 2009. Mycocerosic acid biomarkers for the diagnosis of tuberculosis in the Coimbra skeletal collection. Tuberculosis 89(4): 267-277.

Wilbur AK, Bouwman AS, Stone AC, Roberts CA, Pfister L, Buikstra JE & Brown TA. 2009. Deficiencies and challenges in the study of ancient tuberculosis DNA. J Archaeological Science 36(9): 1990-1997.

Roberts CA, Pfister L & Mays S. 2009. Letter to the editor. Was tuberculosis present in Homo erectus in Turkey? American Journal of Physical Anthropology 139(3): 442-444.

Roberts CA, Buikstra JE 2008 History of tuberculosis from the earliest times to the development of drugs. In PDO Davies, PF Barnes, SB Gordon (eds): Clinical tuberculosis. 4th edition. London, Hodder Arnold, pp. 3-19.

In press

Müller R, Roberts CA, Brown TA Bimolecular identification of ancient Mycobacterium tuberculosis DNA in human remains from Britain and Continental Europe. American J Physical Anthropology

Roberts CA, Buikstra JE. History of tuberculosis from the earliest times to the development of drugs. In PDO Davies, PF Barnes, SB Gordon (eds): Clinical tuberculosis. 5th edition. London, Hodder Arnold

Rubini M, Zaio P, Roberts CA Tuberculosis and leprosy in Italy. New skeletal evidence. Homo

Staff

From the Department of Archaeology