Archaeoparasitology

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Schistosoma haematobium egg Schistosoma haematobium egg 4843 lores.jpg
Schistosoma haematobium egg

Archaeoparasitology, a multi-disciplinary field within paleopathology, is the study of parasites in archaeological contexts. [1] It includes studies of the protozoan and metazoan parasites of humans in the past, as well as parasites which may have affected past human societies, such as those infesting domesticated animals.

Contents

Reinhard suggested that the term "archaeoparasitology" be applied to "... all parasitological remains excavated from archaeological contexts ... derived from human activity" and that "the term 'paleoparasitology' be applied to studies of nonhuman, paleontological material." (p. 233) [2] Paleoparasitology includes all studies of ancient parasites outside of archaeological contexts, such as those found in amber, [3] [4] and even dinosaur parasites. [5]

The first archaeoparasitology report described calcified eggs of Bilharzia haematobia (now Schistosoma haematobium) from the kidneys of an ancient Egyptian mummy. [6] Since then, many fundamental archaeological questions have been answered by integrating our knowledge of the hosts, life cycles and basic biology of parasites, with the archaeological, anthropological and historical contexts in which they are found.

Parasitology basics

Parasites are organisms which live in close association with another organism, called the host, in which the parasite benefits from the association, to the detriment of the host. Many other kinds of associations may exist between two closely allied organisms, such as commensalism or mutualism.

Endoparasites (such as protozoans and helminths), tend to be found inside the host, while ectoparasites (such as ticks, lice and fleas) live on the outside of the host body. Parasite life cycles often require that different developmental stages pass sequentially through multiple host species in order to successfully mature and reproduce. Some parasites are very host-specific, meaning that only one or a few species of hosts are capable of perpetuating their life cycle. Others are not host-specific, since many different hosts appear to harbor and pass on the infective stages of the parasite.

Most archaeoparasitology reports involve species which are considered to be true parasites of humans today. However, incidental parasitism (referred to by some authors as "pseudoparasitism", "false parasitism" or "accidental parasitism") occurs when a parasite which does not normally utilize a host for the perpetuation of its lifecycle is found in that host incidentally. One example is finding the eggs of Cryptocotyle lingua (a fish parasite) in the stomach contents of an Eskimo mummy. [7] It is estimated that 70% of the "parasite" species reported from present-day humans are actually only incidental parasites. [8] Some incidental parasites do cause harm to the infested pseudohosts. [9]

Sources of material

In archaeological contexts, endoparasites (or their eggs or cysts) are usually found in (i) fossilized human or animal dung (coprolites), (ii) the tissues and digestive contents of mummified corpses, [10] or (iii) soil samples from latrines, cesspits, or middens (dumps for domestic waste). A cyst of Echinococcus granulosus was even retrieved from cemetery soil in Poland. [11] Ectoparasites may be found on the skin or scalp, as well as wigs, clothing, or personal grooming accessories found in archaeological sites. [12] [13] Ectoparasite eggs may be found attached to individual hairs. [14] [15] The International Ancient Egyptian Mummy Tissue Bank in Manchester, England, provides tissue samples for a variety of uses, including parasitological studies. [16]

Since 1910, parasite remains have been found in archaeological samples from Africa, the Americas, Asia, Europe, the Middle East, and New Zealand. The age of archaeological sites yielding human parasite remains ranges from approx. 25,000-30,000 years ago [17] to late 19th-early 20th century. [18] Parasite remains have also been found in domestic animal remains at archaeological sites. [19] [20]

Human skeletal remains may exhibit indirect evidence of parasitism. For example, hookworm (Ancyslostoma duodenale) parasitism may lead to anemia, and anemia is one factor associated with the skeletal changes of cribra orbitalia and porotic hyperostosis. Thus, hookworm parasitism may be a causal factor in observed cribra orbitalia and porotic hyperostosis, [21] though dietary factors may also lead to anemia. [22]

Information on the presence of intermediate hosts, required for life cycle completion by many parasites, is also useful in determining the likelihood that a parasite may have infected a particular ancient society. One example is the identification of molluscan intermediate hosts of schistosomiasis in an Islamic archaeological context. [23]

Artifacts depicting the appearance of individuals may also indicate cases of parasitism. Examples include the characteristic facial deformities of leishmaniasis found on pre-Columbian Mochica pottery, [24] and morphological features of certain ancient Egyptian figurative art. [25] Literary sources also provide valuable information regarding not only the parasites present in historic societies, but also the knowledge and attitudes that the people had towards their parasitic infestations. [26] [27] [28] However, specific parasitological diagnoses reported in ancient and medieval texts must always be read with some degree of skepticism. [29]

Techniques and methods

Capillaria hepatica eggs from the corpse of an adolescent from the late Roman period in France, treated with petrographic methods Parasite130094-fig3 Cysts.tif
Capillaria hepatica eggs from the corpse of an adolescent from the late Roman period in France, treated with petrographic methods

Parasite remains in archaeological samples are identified by a variety of techniques. Very durable remains, such as eggs and cysts, may remain intact for many thousands of years. In some cases, relatively intact soft-bodied adult helminths [30] [31] and ectoparasitic arthropods [32] [33] have been found. All of these forms can be identified to the family, genus or species level by compound or electron microscopy.
Petrographic techniques have been used for eggs of Capillaria hepatica found in cysts in the corpse of an adolescent from the late Roman period buried in Amiens (France). [34] The authors stated that identification of tissue-dwelling parasites such as Capillaria hepatica in archaeological remains is particularly dependent on preservation conditions and taphonomic changes and should be interpreted with caution due to morphological similarities with Trichuris sp. eggs

In cases where the intact bodies of parasites are not found, protein or DNA from the parasite may still be present. Antigenic and immunological assays (including enzyme-linked immunoassay - ELISA, [35] [36] [37] ), and DNA sequencing [38] [39] [40] [41] [42] [43] are used to identify the source of these chemical remains, often to the species level.

Fundamental questions

Archaeoparasitological studies have provided information on many fundamental archaeological, historical, and biogeographical questions. These questions may be grouped into the following broad categories: past dietary and farming practices, [44] animal domestication, [45] [46] migration patterns, [47] [48] climate change, [49] sanitary practices, [50] cultural contacts, [51] [52] ethnomedicine, [53] [54] and the overall health of various human societies. [55] Archaeoparasitology data, combined with our knowledge of present host-parasite associations, also contributes to our understanding of the co-evolution of human host-parasite interactions. [56] Our understanding of the geographic origins, evolution and biogeography of the parasites themselves and human diseases associated with them [57] [58] [59] has also benefitted tremendously from archaeoparasitological studies.

Related Research Articles

<span class="mw-page-title-main">Parasitism</span> Relationship between species where one organism lives on or in another organism, causing it harm

Parasitism is a close relationship between species, where one organism, the parasite, lives on or inside another organism, the host, causing it some harm, and is adapted structurally to this way of life. The entomologist E. O. Wilson characterised parasites as "predators that eat prey in units of less than one". Parasites include single-celled protozoans such as the agents of malaria, sleeping sickness, and amoebic dysentery; animals such as hookworms, lice, mosquitoes, and vampire bats; fungi such as honey fungus and the agents of ringworm; and plants such as mistletoe, dodder, and the broomrapes.

<span class="mw-page-title-main">Louse</span> Order of insects

Louse is the common name for any member of the clade Phthiraptera, which contains nearly 5,000 species of wingless parasitic insects. Phthiraptera has variously been recognized as an order, infraorder, or a parvorder, as a result of developments in phylogenetic research.

<i>Ascaris lumbricoides</i> One of several species of Ascaris

Ascaris lumbricoides is a large parasitic worm that causes ascariasis in humans. A roundworm of genus Ascaris, it is the most common parasitic worm in humans. An estimated one-sixth of the human population is at some point infected by a roundworm such as A. lumbricoides; people living in tropical and subtropical countries are at greater risk of infection.

<span class="mw-page-title-main">Head louse</span> Insect parasite of humans

The head louse is an obligate ectoparasite of humans. Head lice are wingless insects that spend their entire lives on the human scalp and feed exclusively on human blood. Humans are the only known hosts of this specific parasite, while chimpanzees and bonobos host a closely related species, Pediculus schaeffi. Other species of lice infest most orders of mammals and all orders of birds.

<span class="mw-page-title-main">Parasitology</span> Study of parasites, their hosts, and the relationship between them

Parasitology is the study of parasites, their hosts, and the relationship between them. As a biological discipline, the scope of parasitology is not determined by the organism or environment in question but by their way of life. This means it forms a synthesis of other disciplines, and draws on techniques from fields such as cell biology, bioinformatics, biochemistry, molecular biology, immunology, genetics, evolution and ecology.

<span class="mw-page-title-main">Hookworm infection</span> Disease caused by intestinal parasites

Hookworm infection is an infection by a type of intestinal parasite known as a hookworm. Initially, itching and a rash may occur at the site of infection. Those only affected by a few worms may show no symptoms. Those infected by many worms may experience abdominal pain, diarrhea, weight loss, and tiredness. The mental and physical development of children may be affected. Anemia may result.

<i>Ascaris</i> Genus of roundworms

Ascaris is a nematode genus of parasitic worms known as the "small intestinal roundworms", which is a type of parasitic worm. One species, Ascaris lumbricoides, affects humans and causes the disease ascariasis. Another species, Ascaris suum, typically infects pigs. Other ascarid genera infect other animals, such as Parascaris equorum, the equine roundworm, and Toxocara and Toxascaris, which infect dogs and cats.

An obligate parasite or holoparasite is a parasitic organism that cannot complete its life-cycle without exploiting a suitable host. If an obligate parasite cannot obtain a host it will fail to reproduce. This is opposed to a facultative parasite, which can act as a parasite but does not rely on its host to continue its life-cycle. Obligate parasites have evolved a variety of parasitic strategies to exploit their hosts. Holoparasites and some hemiparasites are obligate.

Mammomonogamus is a genus of parasitic nematodes of the family Syngamidae that parasitise the respiratory tracts of cattle, sheep, goats, deer, cats, orangutans, and elephants. The nematodes can also infect humans and cause the disease called mammomonogamiasis. Several known species fall under the genus Mammomonogamus, but the most common species found to infest humans is M. laryngeus. Infection in humans is very rare, with only about 100 reported cases worldwide, and is assumed to be largely accidental. Cases have been reported from the Caribbean, China, Korea, Thailand, and Philippines.

<i>Galba truncatula</i> Species of gastropod

Galba truncatula is a species of air-breathing freshwater snail, an aquatic pulmonate gastropod mollusk in the family Lymnaeidae, the pond snails.

<i>Toxascaris leonina</i> Species of roundworm

Toxascaris leonina is a common parasitic roundworm found in dogs, cats, foxes, and related host species. T. leonina is an ascarid nematode, a worldwide distributed helminth parasite which is in a division of eukaryotic parasites that, unlike external parasites such as lice and fleas, live inside their host. The definitive hosts of T. leonina include canids and felines (cats), while the intermediate hosts are usually rodents, such as mice or rats. Infection occurs in the definitive host when the animal eats an infected rodent. While T. leonina can occur in either dogs or cats, it is far more frequent in cats.

<span class="mw-page-title-main">Hemozoin</span>

Haemozoin is a disposal product formed from the digestion of blood by some blood-feeding parasites. These hematophagous organisms such as malaria parasites, Rhodnius and Schistosoma digest haemoglobin and release high quantities of free heme, which is the non-protein component of haemoglobin. Heme is a prosthetic group consisting of an iron atom contained in the center of a heterocyclic porphyrin ring. Free heme is toxic to cells, so the parasites convert it into an insoluble crystalline form called hemozoin. In malaria parasites, hemozoin is often called malaria pigment.

<span class="mw-page-title-main">Paleoparasitology</span> Study of prehistoric parasites

Paleoparasitology is the study of parasites from the past, and their interactions with hosts and vectors; it is a subfield of paleontology, the study of living organisms from the past. Some authors define this term more narrowly, as "Paleoparasitology is the study of parasites in archaeological material." K.J. Reinhard suggests that the term "archaeoparasitology" be applied to "... all parasitological remains excavated from archaeological contexts ... derived from human activity" and that "the term 'paleoparasitology' be applied to studies of nonhuman, paleontological material." This article follows Reinhard's suggestion and discusses the protozoan and animal parasites of non-human animals and plants from the past, while those from humans and our hominid ancestors are covered in archaeoparasitology.

<i>Capillaria aerophila</i> Species of roundworm

Capillaria aerophila is a nematode parasite found in the respiratory tract of foxes, dogs, and various other carnivorous mammals. A few cases of human infestation have also been reported. Though it is sometimes called a "lungworm", this term usually refers to other species of nematodes. Infestation by C. aerophila is referred to as "pulmonary capillariasis", "bronchial capillariasis," or (rarely) "thominxosis." This parasite has a direct life cycle, meaning that the life cycle can be completed in a single host. C. aerophila usually causes only minor clinical symptoms, such as irritation of the respiratory tract and coughing. However, secondary bacterial infections of the respiratory tract, including pneumonia, may develop in heavy infestations. Treatment with anthelmintics, such as levamisole or fenbendazole, is usually sufficient to cure C. aerophila infestations.

<span class="mw-page-title-main">Hookworm vaccine</span>

Hookworm vaccine is a vaccine against hookworm. No effective vaccine for the disease in humans has yet been developed. Hookworms, parasitic nematodes transmitted in soil, infect approximately 700 million humans, particularly in tropical regions of the world where endemic hookworms include Ancylostoma duodenale and Necator americanus. Hookworms feed on blood and those infected with hookworms may develop chronic anaemia and malnutrition. Helminth infection can be effectively treated with benzimidazole drugs, and efforts led by the World Health Organization have focused on one to three yearly de-worming doses in schools because hookworm infections with the heaviest intensities are most common in school-age children. However, these drugs only eliminate existing adult parasites and re-infection can occur soon after treatment. School-based de-worming efforts do not treat adults or pre-school children and concerns exist about drug resistance developing in hookworms against the commonly used treatments, thus a vaccine against hookworm disease is sought to provide more permanent resistance to infection.

<i>Ancylostoma braziliense</i> Species of worm

Ancylostoma braziliense is a species of hookworm belonging to the genus Ancylostoma. It is an intestinal parasite of domestic cats and dogs. Severe infection is often fatal to these pets, especially in puppies and kittens. The infection is particularly endemic in the southern United States. It is most often confused with the zoonotic hookworm species Ancylostoma ceylanicum because of their uncanny resemblance.

<span class="mw-page-title-main">Ancylostomatidae</span> Family of roundworms

The Ancylostomatidae are a family of worms that includes the hookworms.

<span class="mw-page-title-main">Paleofeces</span> Ancient human feces found in archaeological surveys

Paleofeces are ancient human feces, often found as part of archaeological excavations or surveys. The term coprolite is often used interchangeably, although coprolite can also refer to fossilized animal feces. Intact feces of ancient people may be found in caves in arid climates and in other locations with suitable preservation conditions. They are studied to determine the diet and health of the people who produced them through the analysis of seeds, small bones, and parasite eggs found inside. The feces can contain information about the person excreting the material as well as information about the material itself. They can also be chemically analyzed for more in-depth information on the individual who excreted them, using lipid analysis and ancient DNA analysis. The success rate of usable DNA extraction is relatively high in paleofeces, making it more reliable than skeletal DNA retrieval.

<span class="mw-page-title-main">Hookworm</span> Intestinal, blood-feeding, parasitic roundworms that cause types of infection known as helminthiases

Hookworms are intestinal, blood-feeding, parasitic roundworms that cause types of infection known as helminthiases. Hookworm infection is found in many parts of the world, and is common in areas with poor access to adequate water, sanitation, and hygiene. In humans, infections are caused by two main species of roundworm, belonging to the genera Ancylostoma and Necator. In other animals the main parasites are species of Ancylostoma. Hookworm is closely associated with poverty because it is most often found in impoverished areas, and its symptoms promote poverty through the educational and health effects it has on children. It is the leading cause of anemia and undernutrition in developing countries, while being one of the most commonly occurring diseases among poor people. Hookworm thrives in areas where rainfall is sufficient and keeps the soil from drying out, and where temperatures are higher, making rural, coastal areas prime conditions for the parasite to breed.

Cave of Gentio is a parietal art-bearing archaeological site situated about 30 km from Unaí, Minas Gerais, 180 km away from the Federal District.

References

  1. Reinhard KJ, Araújo A (2008). "Archaeoparasitology". In Pearsall, Deborah M. (ed.). Encyclopedia of Archaeology. Amsterdam: Elsevier/Academic Press. pp. 494–501. ISBN   978-0-12-548030-7.
  2. Reinhard KJ (1992). "Parasitology as an interpretive tool in archaeology". Am. Antiq. 57 (2): 231–45. doi:10.2307/280729. JSTOR   280729.
  3. Poinar G.O., Jr.; H. Poinar (2004). "Paleoleishmania proterus n.gen., n.sp. (Trypanosomatidae: Kinetoplastida) from Cretaceous Burmese amber". Protist. 155 (3): 305–10. doi:10.1078/1434461041844259. PMID   15552057.
  4. Wier A, Dolan M, Grimaldi D, Guerrero R, Wagensberg J, Margulis L (February 2002). "Spirochete and protist symbionts of a termite (Mastotermes electrodominicus) in Miocene amber". Proceedings of the National Academy of Sciences of the United States of America. 99 (3): 1410–3. Bibcode:2002PNAS...99.1410W. doi: 10.1073/pnas.022643899 . PMC   122204 . PMID   11818534.
  5. Poinar G, Boucot AJ (August 2006). "Evidence of intestinal parasites of dinosaurs". Parasitology. 133 (Pt 2): 245–9. doi:10.1017/S0031182006000138. PMID   16623965. S2CID   41076534.
  6. Ruffer MA (1910). "Note on the presence of Bilharzia haematobia in Egyptian mummies of the Twentieth Dynasty (1250–1000 BC)". British Medical Journal. 1 (2557): 16. doi:10.1136/bmj.1.2557.16-a. PMC   2330583 . PMID   20764829.
  7. Zimmerman MR (1980). "Aleutian and Alaskan mummies". In Cockburn, Eve; Cockburn, Aidan (eds.). Mummies, disease, and ancient cultures. Cambridge, UK: Cambridge University Press. pp.  118–134. ISBN   978-0-521-23020-9.
  8. Ashford RW (February 1991). "The human parasite fauna: towards an analysis and interpretation". Ann Trop Med Parasitol. 85 (1): 189–98. doi:10.1080/00034983.1991.11812545. PMID   1888215.
  9. Sing A, Tybus K, Fackler I (2008). "Acute urticaria associated with Dicrocoelium dendriticum infestation". Indian J Med Microbiol. 26 (1): 97–8. doi: 10.1016/S0255-0857(21)02013-2 . hdl: 1807/53557 . PMID   18227619.
  10. Nezamabadi M, Mashkour M, Aali A, Stöllner T, Le Bailly M (2013). "Identification of Taeniasp. In a Natural Human Mummy (Third Century BC) from the Chehrabad Salt Mine in Iran". The Journal of Parasitology. 99 (3): 570–572. doi:10.1645/12-113.1. PMID   23240712. S2CID   26253984.
  11. Gladykowska-Rzeczycka JJ, Wrzesinska A, Wrzesinski J (2003). "Rzadkie znalezisko torbieli pasozyta z wczesnosredniowiecznego cmentarzyska w dziekanowicach / A rare finding of a parasitic cyst from an early mediaeval cemetery in Dziekanowice". Archeologia Polski. 48 (1–2): 65–76.
  12. Mumcuoglu YK, Zias J (November 1988). "Head lice, Pediculus humanus capitis (Anoplura: Pediculidae) from hair combs excavated in Israel and dated from the first century B.C. to the eighth century A.D". J. Med. Entomol. 25 (6): 545–7. doi:10.1093/jmedent/25.6.545. PMID   3060619.
  13. Mumcuoglu KY, Zias J, Tarshis M, Lavi M, Stiebel GD (July 2003). "Body louse remains found in textiles excavated at Masada, Israel". J. Med. Entomol. 40 (4): 585–7. doi: 10.1603/0022-2585-40.4.585 . PMID   14680131.
  14. Capasso L, Di Tota G (March 1998). "Lice buried under the ashes of Herculaneum". Lancet. 351 (9107): 992. doi:10.1016/s0140-6736(05)60665-4. PMID   9734976. S2CID   19628629.
  15. Rivera MA, Mumcuoglu KY, Matheny RT, Matheny DG (2008). "Huevecillos de Anthropophthirus capitis en momias de la tradición Chinchorro, Camarones 15-D, norte de Chile / Head lice eggs, Anthropophthirus capitis, from mummies of the Chinchorro tradition, Mamarones 15-D, northern Chile". Chungará – Revista de Antropología Chilena . 40 (1): 30–9. doi: 10.4067/s0717-73562008000100004 .
  16. Lambert-Zazulak PI, Rutherford P, David AR (2003). "The International Ancient Egyptian Mummy Tissue Bank at the Manchester Museum as a resource for the pelaeoepidemiological study of schistosomiasis". World Archaeology. 35 (2): 223–40. doi:10.1080/0043824032000111399. S2CID   162867729.
  17. Bouchet F, Baffier D, Girard M, Morel P, Paicheler J, David F (1996). "Paléoparasitologie en contexte pléistocène premières observations à la Grande Grotte d'Arcy-sur-Cure (Yonne), France". Comptes Rendus de l'Académie des Sciences, Série III. 319 (2): 147–51.
  18. Reinhard KJ, Araújo A, Sianto L, Costello JG, Swope K (February 2008). "Chinese liver flukes in latrine sediments from Wong Nim's property, San Bernardino, California: archaeoparasitology of the Caltrans District Headquarters". J. Parasitol. 94 (1): 300–3. doi:10.1645/GE-1049.1. PMID   18372657. S2CID   12108882.
  19. Dittmar K, Teegen WR (2003). "The presence of Fasciola hepatica (liver-fluke) in humans and cattle from a 4,500-year-old archaeological site in the Saale-Unstrut Valley, Germany" (PDF). Memórias do Instituto Oswaldo Cruz. 98 (Suppl 1): 141–3. doi:10.1590/S0074-02762003000900021. PMID   12687774.
  20. Schelvis J, Koot C (1995). "Sheep or goat? Dalaminia deals with the dilemma". Proceedings of the Section of Experimental and Applied Entomology of the Netherlands Entomological Society. 6: 161–2.
  21. Carlson D, Armelagos G, Van Gerven D (1974). "Factors influencing the etiology of cribra orbitalia in prehistoric Nubia". Journal of Human Evolution. 3 (5): 405–10. doi:10.1016/0047-2484(74)90203-6.
  22. Holland TD, O'Brien MJ (1997). "Parasites, porotic hyperostosis, and the implications of changing perspectives". Am. Antiq. 62 (2): 183–93. doi:10.2307/282505. JSTOR   282505.
  23. Insoll T, Hutchins E (2005). "The archaeology of disease: Molluscs as potential disease indicators in Bahrain" (PDF). World Archaeology. 37 (4): 579–88. doi:10.1080/00438240500411230. S2CID   161727217. Archived from the original (PDF) on 2011-06-27. Retrieved 2008-11-07.
  24. Serarcangeli C, Pennica A (1996). "Testimonianze di una malattia autoctona nella ceramica del Perú precolombiano / Testimonies of an autochthonous illness on the anthropomorphic pottery in ancient Peru". Medicina Nei Secoli. 8 (1): 125–41. PMID   11623468.
  25. Hoeppli R (1973). "Morphological changes in human schistosomiasis and certain analogies in ancient Egyptian sculpture". Acta Tropica. 30 (1): 1–11. doi:10.5169/seals-311865. PMID   4144954.
  26. Moule, Léon (1911). "La parasitologie dans la littérature antique. II. Les parasites du tube digestif". Archives de Parasitologie. 14: 353–83.
  27. Sandison AT (1967). "Parasitic diseases". In Brothwell DR, Sandison AT (eds.). Diseases in Antiquity. Springfield, IL: Charles C. Thomas. pp. 178–183.
  28. Beavis, Ian C. (1988). Insects and other invertebrates in classical antiquity. Exeter: University of Exeter. ISBN   978-0-85989-284-1.
  29. Bondeson J (August 1998). "The bosom serpent". J R Soc Med. 91 (8): 442–7. doi:10.1177/014107689809100817. PMC   1296852 . PMID   9816368.
  30. Allison MJ, Pezzia A, Hasegawa I, Gerszten E (1974). "A case of hookworm infestation in a precolumbian American". American Journal of Physical Anthropology. 41 (1): 103–6. doi:10.1002/ajpa.1330410113. PMID   4602000.
  31. Ferreira LF, Araújo A, Duarte AN (June 1993). "Nematode larvae in fossilized animal coprolites from lower and middle Pleistocene sites, central Italy". J. Parasitol. 79 (3): 440–2. doi:10.2307/3283583. JSTOR   3283583. PMID   8501604.
  32. Araújo A, Ferreira LF, Guidon N, Maues Da Serra Freire N, Reinhard KJ, Dittmar K (July 2000). "Ten thousand years of head lice infection". Parasitol. Today (Regul. Ed.). 16 (7): 269. doi:10.1016/S0169-4758(00)01694-X. PMID   10858638.
  33. Kenward H (April 2001). "Pubic lice in Roman and medieval Britain". Trends Parasitol. 17 (4): 167–8. doi:10.1016/S1471-4922(01)01890-6. PMID   11360885.
  34. Mowlavi, G.; Kacki, S.; Dupouy-Camet, J.; Mobedi, I.; Makki, M.; Harandi, MF.; Naddaf, SR. (2014). "Probable hepatic capillariosis and hydatidosis in an adolescent from the late Roman period buried in Amiens (France)". Parasite. 21: 9. doi:10.1051/parasite/2014010. PMC   3936287 . PMID   24572211. Open Access logo PLoS transparent.svg
  35. Deelder AM, Miller RL, de Jonge N, Krijger FW (March 1990). "Detection of schistosome antigen in mummies". Lancet. 335 (8691): 724–5. doi:10.1016/0140-6736(90)90838-V. PMID   1969079. S2CID   12113260.
  36. Gonçalves ML, Araújo A, Duarte R, et al. (2002). "Detection of Giardia duodenalis antigen in coprolites using a commercially available enzyme-linked immunosorbent assay". Trans. R. Soc. Trop. Med. Hyg. 96 (6): 640–3. doi:10.1016/S0035-9203(02)90337-8. PMID   12625140.
  37. Mitchell PD, Stern E, Tepper Y (2008). "Dysentery in the crusader kingdom of Jerusalem: An ELISA analysis of two medieval latrines in the City of Acre (Israel)". Journal of Archaeological Science. 35 (7): 1849–53. doi:10.1016/j.jas.2007.11.017.
  38. Aufderheide AC, Salo W, Madden M, et al. (February 2004). "A 9,000-year record of Chagas' disease". Proceedings of the National Academy of Sciences of the United States of America. 101 (7): 2034–9. Bibcode:2004PNAS..101.2034A. doi: 10.1073/pnas.0307312101 . PMC   357047 . PMID   14766963.
  39. Dittmar K, Mamat U, Whiting M, Goldmann T, Reinhard K, Guillen S (2003). "Techniques of DNA-studies on prehispanic ectoparasites (Pulex sp., Pulicidae, Siphonaptera) from animal mummies of the Chiribaya culture, southern Peru". Memórias do Instituto Oswaldo Cruz. 98 (Suppl 1): 53–8. doi: 10.1590/S0074-02762003000900010 . PMID   12687763.
  40. Iñiguez AM, Reinhard K, Carvalho Gonçalves ML, Ferreira LF, Araújo A, Paulo Vicente AC (November 2006). "SL1 RNA gene recovery from Enterobius vermicularis ancient DNA in pre-Columbian human coprolites". Int. J. Parasitol. 36 (13): 1419–25. doi:10.1016/j.ijpara.2006.07.005. PMID   16950265.
  41. Loreille O, Roumat E, Verneau O, Bouchet F, Hänni C (August 2001). "Ancient DNA from Ascaris: extraction amplification and sequences from eggs collected in coprolites". Int. J. Parasitol. 31 (10): 1101–6. doi:10.1016/S0020-7519(01)00214-4. PMID   11429174.
  42. Raoult D, Reed DL, Dittmar K, et al. (February 2008). "Molecular identification of lice from pre-Columbian mummies". J. Infect. Dis. 197 (4): 535–43. doi: 10.1086/526520 . PMID   18254682.
  43. Zink AR, Spigelman M, Schraut B, Greenblatt CL, Nerlich AG, Donoghue HD (October 2006). "Leishmaniasis in ancient Egypt and Upper nubia". Emerging Infect. Dis. 12 (10): 1616–7. doi:10.3201/eid1210.060169. PMC   3290941 . PMID   17176592.
  44. Reinhard KJ, Hevly RH, Anderson GA (June 1987). "Helminth remains from prehistoric Indian coprolites on the Colorado Plateau". J. Parasitol. 73 (3): 630–9. doi:10.2307/3282147. JSTOR   3282147. PMID   3298603.
  45. Nansen P, Jorgensen RJ (June 1977). "[Parasite eggs identified in material from archaeological excavations in Ribe (the viking age) (author's transl)]". Nord Vet Med (in Danish). 29 (6): 263–6. PMID   896405.
  46. Sadler JP (July 1990). "Records of ectoparasites on humans and sheep from Viking-age deposits in the former western settlement of Greenland". J. Med. Entomol. 27 (4): 628–31. doi:10.1093/jmedent/27.4.628. PMID   2201769.
  47. Araujo A, Reinhard KJ, Ferreira LF, Gardner SL (March 2008). "Parasites as probes for prehistoric human migrations?". Trends Parasitol. 24 (3): 112–5. doi:10.1016/j.pt.2007.11.007. PMID   18262843.
  48. Montenegro A, Araújo A, Eby M (2006). "Parasites, paleoclimate, and the peopling of the Americas: Using the hookworm to time the Clovis migration". Current Anthropology. 47 (1): 193–200. doi:10.1086/499553.
  49. Araújo A, Rangel A, Ferreira LF (1993). "Climatic change in northeastern Brazil: Paleoparasitological data". Memórias do Instituto Oswaldo Cruz. 88 (4): 577–9. doi: 10.1590/S0074-02761993000400014 .
  50. Faulkner CT (1991). "Prehistoric diet and parasitic infection in Tennessee: Evidence from the analysis of desiccated human paleofeces". Am. Antiq. 56 (4): 687–700. doi:10.2307/281546. JSTOR   281546.
  51. Araújo A, Ferreira LF, Confalonieri U, Chame M (1988). "Hookworms and the peopling of America". Cadernos de Saúde Pública. 4 (2): 226–33. doi: 10.1590/S0102-311X1988000200006 .
  52. Bouchet F, Harter S, Paicheler JC, Aráujo A, Ferreira LF (April 2002). "First recovery of Schistosoma mansoni eggs from a latrine in Europe (15-16th centuries)". J. Parasitol. 88 (2): 404–5. doi:10.1645/0022-3395(2002)088[0404:FROSME]2.0.CO;2. PMID   12054021.
  53. Reinhard KJ, Ambler JR, McGuffie M (1985). "Diet and parasitism at Dust Devil Cave". Am. Antiq. 50 (4): 819–24. doi:10.2307/280170. JSTOR   280170.
  54. Chaves S.A.; de M.; K.J. Reinhard (2006). "Critical analysis of coprolite evidence of medicinal plant use in Piaui, Brazil". Palaeogeography, Palaeoclimatology, Palaeoecology. 237 (1): 110–8. doi:10.1016/j.palaeo.2005.11.031.
  55. Sallares, Robert (2002). Malaria and Rome: a history of malaria in ancient Italy. Oxford [Oxfordshire]: Oxford University Press. ISBN   978-0-19-924850-6.
  56. Ashford RW (1 September 2000). "Parasites as indicators of human biology and evolution". J. Med. Microbiol. 49 (9): 771–2. doi:10.1099/0022-1317-49-9-771. PMID   10966223.[ permanent dead link ]
  57. Hugot JP, Reinhard KJ, Gardner SL, Morand S (September 1999). "Human enterobiasis in evolution: origin, specificity and transmission". Parasite. 6 (3): 201–8. doi: 10.1051/parasite/1999063201 . PMID   10511967.
  58. Nozais JP (2003). "The origin and dispersion of human parasitic diseases in the old world (Africa, Europe and Madagascar)". Mem. Inst. Oswaldo Cruz. 98 (Suppl 1): 13–9. doi: 10.1590/S0074-02762003000900004 . PMID   12687757.
  59. Hoberg EP (2006). "Phylogeny of Taenia: Species definitions and origins of human parasites". Parasitol. Int. 55 (Suppl): S23–30. doi:10.1016/j.parint.2005.11.049. PMID   16371252.