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The intestinal parasites of King Richard III

DOI:10.1016/S0140-6736(13)61757-2
Authors:
Piers D Mitchell at University of Cambridge
Piers D Mitchell
Ivy Hui-Yuan Yeh 葉惠媛 at Nanyang Technological University
Ivy Hui-Yuan Yeh 葉惠媛
Jo Appleby at University of Leicester
Jo Appleby
Richard Buckley
Richard Buckley
Richard Buckley
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1
The Intestinal Parasites of King Richard III
Authors:
Piers D. Mitchell MD,1* Hui-Yuan Yeh MA,1 Jo Appleby PhD,2 Richard Buckley
BA,3
1 Division of Biological Anthropology, Department of Archaeology and
Anthropology, University of Cambridge, The Henry Wellcome Building,
Fitzwilliam Street, Cambridge, CB2 1QH, UK.
2 School of Archaeology and Ancient History, University of Leicester,
University Road, Leicester, LE1 7RH, UK.
3 University of Leicester Archaeological Services, University of Leicester,
University Road, Leicester, LE1 7RH, UK.
*Correspondiong Author: Dr. Piers Mitchell, Division of Biological Anthropology,
Department of Archaeology and Anthropology, University of Cambridge, The
Henry Wellcome Building, Fitzwilliam Street, Cambridge, CB2 1QH, UK. e-mail:
pdm39@cam.ac.uk
Mitchell, P.D., Yeh, H.-Y., Appleby, J., Buckley, R. 2013. The intestinal parasites of King Richard III.
The Lancet 382: 888.
Unformatted Copy of the Following Article
2
The Intestinal Parasites of King Richard III
Richard III ruled England from 1483-85 AD, and he died at the battle of Bosworth
Field near Leicester. He is one of England’s most well known medieval kings
because of his portrayal as a villain in Shakespeare’s play Richard III, in part a
consequence of his usurping the throne and the perception of his spinal
deformity. His body was buried in the church of the friars minor (Grey Friars) in
Leicester.1 In September 2012 Richard’s remains were excavated and sediment
samples were taken from the sacral area of his pelvis, and control samples from
his skull and the soil outside the grave cut (figure 1). Analysis was done with
disaggregation with trisodium phosphate, microsieving with 300, 160, and 20µm
diameter mesh, and then light microscopy.2 The results showed the presence of
multiple roundworm eggs (Ascaris lumbricoides) in the sacral sample, where the
intestines would have been during life (figure 2). The eggs were decorticated and
dimensions ranged from 55.1-69.8 µm in length to 40.9-48.2 µm in breadth. The
control sample from the skull was negative for parasite eggs, and the control
sample from outside the grave cut shows only scanty environmental soil
contamination with parasite eggs.
These results show that Richard was infected with roundworms in his
intestines. Roundworm is spread by the faecal contamination of food by dirty
hands, or use of faeces as a crop fertiliser. No other species of intestinal parasite
were present in the samples. Past research into human intestinal parasites in
Britain was shown a number of species to have been present prior to the
3
medieval period, including roundworm (Ascaris lumbricoides), whipworm
(Trichuris trichiura), beef/pork tapeworm (Taenia saginata/solium), fish tapeworm
(Diphyllobothrium latum), and liver fluke (Fasciola hepatica). We would expect
nobles of this period to have eaten meats such as beef, pork and fish regularly,
but there was no evidence for the eggs of the beef, pork or fish tapeworm. This
may suggest that his food was cooked thoroughly, which would have prevented
the transmission of these parasites.
Funding: University of Leicester, Richard III society, Leicester City Council,
Leicester Shire Promotions, Leicester Adult Schools.
References
1 Buckley R, Morris M, Appleby J, King T, O’Sullivan D, Foxhall L. ‘The king in the
car park’: new light on the death and burial of Richard III in the Grey Friars
church, Leicester in 1485. Antiquity 2013; 87: 519-38.
2 Anastasiou E, Mitchell PD. Simplifying the process for extracting parasitic worm
eggs from cesspool and latrine sediments: a trial comparing the efficacy of widely
used techniques for disaggregation. International Journal of Paleopathology
doi:10.1016/j.ijpp.2013.04.004.
4
List of Figures
Figure 1: Skeleton of Richard at excavation, with sampling locations marked. s –
sacral sample, c1 – skull control sample, c2 – control sample from outside grave
5
Figure 2: Decorticated roundworm egg (Ascaris lumbricoides) from sacral sample
of Richard III. Dimensions 64.1 x 45.6µm. Bar measures 20µm.
6
Authors Contributions
PM designed the study, performed the bulk of the parasite analysis, performed
the background research and wrote the article, HYY performed some of the
parasite analysis, JB excavated the skeleton and took the samples, and RB led
the entire excavation project.
Role of Funding Source
The research was funded by the University of Leicester, Richard III Society,
Leicester City Council, Leicester Shire Promotions, and Leicester Adult Schools.
While they funded the excavations and post excavation analysis of the remains
from the Grey Friars church, they had no influence on what research was
undertaken, nor on the interpretation of the results from that research.
Ethics Committee Approval
No ethics committee approval was required since the study did not involve
patients. The UK Minstry of Justice issued a licence permitting the excavation.
Conflict of Interest Statement
The authors have no conflict of interest to declare.
... Intestinal helminths are often identified in archaeological excavations because the eggs are environmentally resilient and remain identifiable by morphology for thousands of years (e.g. [10][11][12][13][14][15][16][17][18]). Helminth eggs can be identified to the genus level by light microscopy [19] and their presence indicates infection of a host with adult parasites. ...
... Helminth eggs have been detected archaeologically in different types of faecal-associated material including latrines and other communal deposits (e.g. waste ditches), and samples associated with single individuals (e.g. the abdominal region of mummified or skeletal remains [11,14,17,[20][21][22][23][24][25][26][27]. The detection of parasites in each type of context provides different kinds of information. ...
... The High/Late Medieval period represented a peak in prevalence rates in England with overall lower numbers detected in samples dated from the Anglo-Saxon/Early Medieval period (albeit with variation between sites). The eggs of both parasites are readily detected in communal medieval deposits from the UK and often found in high numbers [14,46,47,51,[58][59][60][61][62][63][64][65][66][67][68]. Unfortunately, the data was often not quantitative or based on single samples, which makes it difficult to compare between studies. ...
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... Intestinal helminths have afflicted humans throughout history and their robust eggs are detectable in a wide range of archaeological contexts [1][2][3][4][5][6][7]. In modern times soil transmitted helminths (STH) affect more than 1.5 billion people worldwide, mostly in Less Economically Developed Countries [8][9][10]. ...
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... In modern endemic populations, STH infections are associated with poverty, being considered an indicator of insufficient access to sanitation and clean drinking water [48]. However, in past populations, these parasites infected humans in all sectors of society, including the wealthy and privileged [20,49,50]. The royalsocietypublishing.org/journal/rstb Phil. ...
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Enteric helminths are common parasites in many parts of the world and in the past were much more widespread both geographically and socially. Many enteric helminths are relatively long-lived in the human host, often benign or of low pathogenicity while producing large numbers of environmentally resistant eggs voided in the faeces or found associated with individual remains (skeletons and mummies). The combination of helminth characters offers opportunities to the field of historical pathogen research that are quite different to that of some of the more intensively studied high impact pathogens. Historically, a wealth of studies has employed microscopic techniques to diagnose infection using the morphology of the helminth eggs. More recently, various ancient DNA (aDNA) approaches have been applied in the archaeoparasitological context and these are revolutionizing the field, allowing much more specific diagnosis as well as interrogating the epidemiology of helminths. These advances have enhanced the potential for the field to provide unique information on past populations including using diseases to consider many aspects of life (e.g. sanitation, hygiene, diet, culinary practices and other aspects of society). Here, we consider the impact of helminth archaeoparasitology and more specifically the impact and potential for application of aDNA technologies as a part of the archaeologists' toolkit. This article is part of the theme issue ‘Insights into health and disease from ancient biomolecules’.
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Ancient parasite studies depend on the recovery of parasite remains from archaeological material. Collection strategies, sample processing, and the use of parasitological techniques are essential to perform the analyses without loss of microremains and also to interpret the data obtained by correlating with the archaeological information. Together with the methods of analyses, the identification and differentiation between these microremains and others commonly observed in the processed samples, such as pollen grains, plant spores, fungi spores, and others, are essential so that no misdiagnosis occurs, resulting in misinterpretation of the health situation of an ancient population. All ancient parasite studies require an evaluation and discussion of taphonomy, based on the factors identified in each archaeological site. Paleoparasitology does not only require the identification of parasite remains in samples, but it involves a set of strategies, meticulous training, and application of multiple concepts in order to clarify the infection/disease process in ancient populations. In this chapter, the importance of paleoparasitology is discussed, and strategies and recommendations on sample collection, sample processing, use of parasitological techniques, and researcher training are presented. Taphonomic aspects related to experimental studies in specific sites are discussed. This chapter aims to orient those interested in the field and guide the community toward establishing principles of preservation applicable in all types of archaeological remains in which eggs can be recovered.
... During historic periods, human populations living in crowded towns and cities, with inadequate sanitation were subject to high levels of parasitism, as attested by the recovery of the eggs of giant roundworm (Ascaris lumbricoides), whipworm (Trichuris trichiura) and tapeworms (e.g., Taenia solium, Taenia saginata, Diphyllobothrium latum) at numerous sites worldwide (e.g., Leles et al. 2010;Mitchell et al. 2013;Yeh et al. 2014). Although eggs of these intestinal worms are probably the most commonly recovered parasite remains, careful screening of latrine and midden deposits can favour the recovery of a wide range of parasitic taxa that inform us on diseases that afflicted people in the past, as well as on the foods that may have ingenerated such health problems. ...
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Mitchell, P.D. Sampling human remains for evidence of intestinal parasites. In: Mitchell, P.D., Brickley, M. (eds) Updated Guidelines to the Standards for Recording Human Remains. Chartered Institute for Archaeologists/British Association for Biological Anthropology and Osteoarchaeology: Reading, 2017, p.54-56. ISBN 978-0-948393-27-3
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'The king in the car park': New light on the death and burial of Richard III in the Grey Friars church, Leicester, in 1485
Article
Full-text available
  • Jun 2015
Archaeologists today do not as a rule seek to excavate the remains of famous people and historical events, but the results of the project reported in this article provide an important exception. Excavations on the site of the Grey Friars friary in Leicester, demolished at the Reformation and subsequently built over, revealed the remains of the friary church with a grave in a high status position beneath the choir. The authors set out the argument that this grave can be associatedwith historical records indicating that Richard III was buried in this friary after his death at the Battle of Bosworth. Details of the treatment of the corpse and the injuries that it had sustained support their case that this should be identified as the burial of the last Plantagenet king. This paper presents the archaeological and the basic skeletal evidence: the results of the genetic analysis and full osteoarchaeological analysis will be published elsewhere.
Simplifying the process of extracting intestinal parasite eggs from archaeological sediment samples: A comparative study of the efficacy of widely-used disaggregation techniques
Article
Full-text available
  • Sep 2013
Some scientific techniques are widely used because they work satisfactorily, but they may not be the cheapest, fastest or most efficient method possible. Here we assess the widely used methods for disaggregating archaeological latrine sediments, where solid soils are converted to aqueous suspension prior to microscopic analysis for ancient parasite eggs. It has been noted that there is great variability in protocols described in the published literature. We have used samples from a medieval latrine in Cyprus and a cesspool from Israel containing roundworm eggs to evaluate in a pilot study whether there appears to be distinct advantages to any of the standard protocols. The results suggest that there is very little difference in the efficacy whether disaggregation is performed using traditional 0.5% trisodium phosphate or simple distilled water, whether the process lasts 72 h or just 1 h, or whether sonication is added to the process. While a larger sample size would allow a more robust statistical analysis, this pilot study provides no evidence to suggest the long disaggregation periods, expensive chemicals, or sonication steps leads to any better disaggregation in latrine sediments than using distilled water for just 1 h.
Simplifying the process for extracting parasitic worm eggs from cesspool and latrine sediments: a trial comparing the efficacy of widely used techniques for disaggregation
  • May 2013
  • E Anastasiou
  • P D Mitchell
Anastasiou E, Mitchell PD. Simplifying the process for extracting parasitic worm eggs from cesspool and latrine sediments: a trial comparing the efficacy of widely used techniques for disaggregation. Int J Paleopathol 2013; published online May 29. DOI:10.1016/j.ijpp.2013.04.004. Figure: The intestinal parasites of King Richard III (A) Skeleton of Richard III at excavation, with sampling locations marked. S=sacral sample. C1=skull control sample. C2=control sample from outside grave.
Decorticated roundworm egg (Ascaris lumbricoides) from sacral sample of Richard III. Dimensions 64·1×45·6 μm
  • Jan 2013
  • LANCET
  • 888
Decorticated roundworm egg (Ascaris lumbricoides) from sacral sample of Richard III. Dimensions 64·1×45·6 μm. Lancet 2013; 382: 888 Published Online September 4, 2013