Archaeoparasitology

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.

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, 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.[10] Ectoparasites may be found on the skin or scalp, as well as wigs, clothing, or personal grooming accessories found in archaeological sites.[11][12] Ectoparasite eggs may be found attached to individual hairs.[13][14] The International Ancient Egyptian Mummy Tissue Bank in Manchester, England, provides tissue samples for a variety of uses, including parasitological studies.[15]

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[16] to late 19th-early 20th century.[17] Parasite remains have also been found in domestic animal remains at archaeological sites.[18][19]

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,[20] though dietary factors may also lead to anemia.[21]

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.[22]

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,[23] and morphological features of certain ancient Egyptian figurative art.[24] 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.[25][26][27] However, specific parasitological diagnoses reported in ancient and medieval texts must always be read with some degree of skepticism.[28]

Techniques and methods

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[29][30] and ectoparasitic arthropods[31][32] 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).[33] 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,[34][35][36]), and DNA sequencing[37][38][39][40][41][42] 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,[43] animal domestication,[44][45] migration patterns,[46][47] climate change,[48] sanitary practices,[49] cultural contacts,[50][51] ethnomedicine,[52][53] and the overall health of various human societies.[54] 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.[55] Our understanding of the geographic origins, evolution and biogeography of the parasites themselves and human diseases associated with them[56][57][58] has also benefitted tremendously from archaeoparasitological studies.

References

  1. ↑ Reinhard KJ, Araújo A (2008). "Archaeoparasitology". In Pearsall, Deborah M. Encyclopedia of Archaeology. Amsterdam: Elsevier/Academic Press. pp. 494–501. ISBN 0-12-548030-X.
  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. and H. Poinar (2004). "Paleoleishmania proterus n.gen., n.sp. (Trypanosomatidae: Kinetoplastida) from Cretaceous Burmese amber". Protista 155 (3): 305–10. doi:10.1078/1434461041844259.
  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. 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.
  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.
  7. ↑ Zimmerman MR (1980). "Aleutian and Alaskan mummies". In Cockburn, Eve; Cockburn, Aidan. Mummies, disease, and ancient cultures. Cambridge, UK: Cambridge University Press. pp. 118–134. ISBN 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. 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:10.4103/0255-0857.38879. PMID 18227619.
  10. ↑ 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.
  11. ↑ 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. PMID 3060619.
  12. ↑ 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.
  13. ↑ 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.
  14. ↑ 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.
  15. ↑ 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.
  16. ↑ 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 des Seances de l'Academie des Sciences. Série III. Sciences de la Vie 319 (2): 147–51.
  17. ↑ 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.
  18. ↑ 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.
  19. ↑ 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.
  20. ↑ Carlson D, Armelagos G, Van Gerven D (1974). "Factors influencing the etiology of cribra orbitalia in prehistoric Nubia". Journal of Human Evolution 3 (3): 405–10. doi:10.1016/0047-2484(74)90203-6.
  21. ↑ 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.
  22. ↑ 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.
  23. ↑ 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.
  24. ↑ Hoeppli R (1973). "Morphological changes in human schistosomiasis and certain analogies in ancient Egyptian sculpture". Acta Tropica 30 (1): 1–11. PMID 4144954.
  25. ↑ Moule, Léon (1911). "La parasitologie dans la litterature antique. II. Les parasites du tube digestif". Archives de Parasitologie 14: 353–83.
  26. ↑ Sandison AT (1967). "Parasitic diseases". In Brothwell DR, Sandison AT. Diseases in Antiquity. Springfield, IL: Charles C. Thomas. pp. 178–183.
  27. ↑ Beavis, Ian C. (1988). Insects and other invertebrates in classical antiquity. Exeter: University of Exeter. ISBN 0-85989-284-0.
  28. ↑ Bondeson J (August 1998). "The bosom serpent". J R Soc Med 91 (8): 442–7. PMC 1296852. PMID 9816368.
  29. ↑ 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.
  30. ↑ 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.
  31. ↑ 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.
  32. ↑ 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.
  33. ↑ 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.
  34. ↑ 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.
  35. ↑ 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.
  36. ↑ 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.
  37. ↑ 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. doi:10.1073/pnas.0307312101. PMC 357047. PMID 14766963.
  38. ↑ 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.
  39. ↑ 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.
  40. ↑ 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.
  41. ↑ 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?url_ver=Z39.88-2003&rfr_id=ori:rid:crossref.org&rfr_dat=cr_pub=ncbi.nlm.nih.gov. PMID 18254682.
  42. ↑ 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.
  43. ↑ 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.
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  45. ↑ 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. PMID 2201769.
  46. ↑ 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.
  47. ↑ 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.
  48. ↑ 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.
  49. ↑ 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.
  50. ↑ 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.
  51. ↑ 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.
  52. ↑ 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.
  53. ↑ Chaves S.A., de M. and 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.
  54. ↑ Sallares, Robert (2002). Malaria and Rome: a history of malaria in ancient Italy. Oxford [Oxfordshire]: Oxford University Press. ISBN 0-19-924850-8.
  55. ↑ Ashford RW (1 September 2000). "Parasites as indicators of human biology and evolution". J. Med. Microbiol. 49 (9): 771–2. PMID 10966223.
  56. ↑ 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.
  57. ↑ 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.
  58. ↑ 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.
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