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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
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Figure 2: Decorticated roundworm egg (Ascaris lumbricoides) from sacral sample
of Richard III. Dimensions 64.1 x 45.6µm. Bar measures 20µm.
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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 helminth parasites (worms) have afflicted humans throughout history and their eggs are readily detected in archaeological deposits including at locations where intestinal parasites are no longer considered endemic (e.g. the UK). Parasites provide valuable archaeological insights into historical health, sanitation, hygiene, dietary and culinary practices, as well as other factors. Differences in the prevalence of helminths over time may help us understand factors that affected the rate of infection of these parasites in past populations. While communal deposits often contain relatively high numbers of parasite eggs, these cannot be used to calculate prevalence rates, which are a key epidemiological measure of infection. The prevalence of intestinal helminths was investigated through time in England, based on analysis of 464 human burials from 17 sites, dating from the Prehistoric to Industrial periods. Eggs from two faecal-oral transmitted nematodes (Ascaris sp. and Trichuris sp.) and the food-derived cestodes (Taenia spp. and Diphyllobothrium latum syn Dibothriocephalus latus) were identified, although only Ascaris was detected at a high frequency. The changing prevalence of nematode infections can be attributed to changes in effective sanitation or other factors that affect these faecal-oral transmitted parasites and the presence of cestode infections reflect dietary and culinary preferences. These results indicate that the impact of helminth infections on past populations varied over time, and that some locations witnessed a dramatic reduction in parasite prevalence during the industrial era (18th-19th century), whereas other locations continued to experience high prevalence levels. The factors underlying these reductions and the variation in prevalence provide a key historical context for modern anthelmintic programs.
... 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]. ...
... Helminth eggs are robust and can be identified in a wide range of archaeological samples including the abdominal region of mummified bodies and skeletal remains as well as communal waste pits or latrines using microscopic techniques (e.g. [2,6,26,27]). Egg morphology is adequate for genus-level diagnosis, while molecular approaches can be employed to identify species [1,7,28,29]. The two nematodes Ascaris sp. and Trichuris trichiura are both among the most prevalent STH in modern populations and also widely reported in archaeological sites (e.g. ...
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Helminth infections are among the World Health Organization’s top neglected diseases with significant impact in many Less Economically Developed Countries. Despite no longer being endemic in Europe, the widespread presence of helminth eggs in archaeological deposits indicates that helminths represented a considerable burden in past European populations. Prevalence of infection is a key epidemiological feature that would influence the elimination of endemic intestinal helminths, for example, low prevalence rates may have made it easier to eliminate these infections in Europe without the use of modern anthelminthic drugs. To determine historical prevalence rates we analysed 589 grave samples from 7 European sites dated between 680 and 1700 CE, identifying two soil transmitted nematodes (Ascaris spp. and Trichuris trichiura) at all locations, and two food derived cestodes (Diphyllobothrium latum and Taenia spp.) at 4 sites. The rates of nematode infection in the medieval populations (1.5 to 25.6% for T. trichiura; 9.3–42.9% for Ascaris spp.) were comparable to those reported within modern endemically infected populations. There was some evidence of higher levels of nematode infection in younger individuals but not at all sites. The genetic diversity of T. trichiura ITS-1 in single graves was variable but much lower than with communal medieval latrine deposits. The prevalence of food derived cestodes was much lower (1.0–9.9%) than the prevalence of nematodes. Interestingly, sites that contained Taenia spp. eggs also contained D. latum which may reflect local culinary practices. These data demonstrate the importance of helminth infections in Medieval Europe and provide a baseline for studies on the epidemiology of infection in historical and modern contexts. Since the prevalence of medieval STH infections mirror those in modern endemic countries the factors affecting STH decline in Europe may also inform modern intervention campaigns.
... 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’.
... Similarly, the presence of pinworms (Enterobius vermicularis) suggests personal hygiene challenges and cramped living conditions. Findings of fecal-borne parasites as a result of poor sanitation practices have been documented throughout time and in many locations (Reinhard et al. 1986;Faulkner 1991;Warnock and Reinhard 1992;Reinhard 2017;Matsui et al. 2003;Mitchell 2015), with a recent strong focus in the Roman and Medieval periods (Mitchell and Tepper 2008;Mitchell et al. , 2011Mitchell et al. , 2013Yeh et al. 2014;Mitchell 2017). Since 2016, researchers in central Russia and Siberia defined new patterns in infection. ...
Chapter
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. ...
... The best location for sampling a supine burial for intestinal parasites is to take soil from the anterior aspect of the sacrum, and from the sacral foramina (Fugassa et al 2008;Le Bailly et al 2006;Mitchell et al 2013). This is because the contents of the decomposed intestines will move posteriorly over time due to gravity. ...
Chapter
Full-text available
When an individual dies and is buried in the soil, the soft tissues decompose over the following months. The intestines are located in the pelvis and abdomen, and their contents will be released into the soil as they break down. If there are intestinal parasites present, the worms (helminths) die once the host dies, and soil organisms consume them. However, the eggs of intestinal parasitic worms often have a tough, chitinous cell wall that prevents their decomposition by soil bacteria and fungi. The eggs themselves will become unviable after a year or two in the soil, so do not pose any risk of infecting the archaeologist who excavates the burial. Study of ancient parasites is helpful as it not only helps us determine patterns of disease in past populations, but can also enable us to understand the evolutionary spread of infectious diseases, the levels of sanitation in past communities, the components of ancient diet, provide evidence for migrations, and sometimes indicate occupational activities.
... Similarly, the presence of pinworms (Enterobius vermicularis) suggests personal hygiene challenges and cramped living conditions. Findings of fecal-borne parasites as a result of poor sanitation practices have been documented throughout time and in many locations (Reinhard et al. 1986;Faulkner 1991;Warnock and Reinhard 1992;Reinhard 2017;Matsui et al. 2003;Mitchell 2015), with a recent strong focus in the Roman and Medieval periods (Mitchell and Tepper 2008;Mitchell et al. , 2011Mitchell et al. , 2013Yeh et al. 2014;Mitchell 2017). Since 2016, researchers in central Russia and Siberia defined new patterns in infection. ...
Preprint
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 occur, resulting in misinterpretation of the health situation of an ancient population. All ancient parasite studies require taphonomy evaluation and discussion, 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, strategies and recommendations on sample collection, sample processing, use of parasitological techniques and researcher training are pointed. Taphonomic aspects
Thesis
Paleoparasitological data on the Iberian Peninsula is in particular scarce. This work provides an introduction to the field of Paleoparasitology, demonstrates the application of its techniques in archaeological contexts and adds to the knowledge of the disease in the past. To achieve this, we constructed ancient parasite eggs sampling strategies, soil-sampled and tested three Neolithic sites: El Mirador cave (fumiers deposits) (c. 5300-3500 cal. BC), Can Sadurní cave (fumiers deposits) (4709-4555 cal. BC), and La Draga (5300-4700 cal. BC) permanent open-air settlement (cultural layer, sector A). In total, we collected 109 samples, represented as a 6513 g of sediment. Analysis results provided in this work are based on 46 fully processed and analysed samples. La Draga site remains to be the only parasitological data providing lakeside settlement associated with the Mediterranean route of Neolitization with our new findings of Trichuris sp. and Taenia or Echinococcus sp. We consider our study of El Mirador and Can Sadurní fumiers deposits to stand for one of the first paleoparasitological works in the contexts of the fumiers in general. Analysed deposits from both caves tested negative for ancient parasite eggs presence. In this work, we argue that negative samples could potentially indicate false negatives due to the burning practices in the caves and do not display the absence of the infection.
Chapter
DNA is the abbreviation for deoxyribonucleic acid. It involves the hereditary information for humans and other organisms. The DNA is based in the cell nucleus but also in the mitochondria. The chemical bases of the DNA are adenine (A), guanine (G), cytosine (C) and thymine (T). The sequence of these bases is decisive for the makeup of organisms. The bases are connected to sugar and phosphate called nucleotide. They are formed to a spiral which is also known as double helix. The fact that DNA can replicate makes life possible. In 1869 Friedrich Miescher isolated DNA for the first time. In 1953 Francis Crick and James Watson presented their double-helix model of DNA based on an x-ray photo of Rosalind Franklin and Raymond Gosling. Francis Crick and James Watson received in 1962 the Nobel Prize in Physiology and Medicine.
Book
Cambridge Core - Archaeology: General Interest - The Archaeology of Food - by Katheryn C. Twiss
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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.
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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
  • 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
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