Paleoparasitology and Paleogeography - ancient parasite infections in the Old World and its influence in the colonial America

Adauto Araújo, Daniela Leles, Luciana Sianto, Françoise Bouchet, Matthieu Le Bailly, Alena Iñiguez,

Martín Fugassa, Karl Reinhard, Sheila Mendonça de Souza, Luiz Fernando Ferreira

Oswaldo Cruz Foundation, Rio de Janeiro, BrasilUniversité de Reims, FranceUniversity of Nebraska, USA

Universidad Nacional de Mar del Plata, Argentina

Some parasites infecting humans today date from African ancestors

Pinworm egg (Enterobius vermicularis) found in a human coprolite dated of 6,000 years, Chile

Pediculus humanus (head lice) found in a partially mummified human body, Brazil, dated of 12,000 years.

Other parasites were acquired during the history of human biological and cultural evolution

Ipanema beach, Rio de Janeiro, Brasil

Plant and animal domestication brought new parasites

With agriculture, wild animals were attracted closer to humans.

Consequently, new parasites emerged after adapting to the human host

Population growth occurred

People stayed in the same places for more time

Human population dispersed through the world

Humans migrated from Africa to other territories, conquering and transforming the places they choose to settle

Parasites inherited from human ancestors migrated with their hosts

Some parasite species were able to maintain their life cycles in new environments, whereas others were lost and disappeared

http://learn.genetics.utah.edu/content/begin/cells/organelles/> (13 June 2010)

Paleoparasitology

Luiz Fernando Ferreira, at the Oswaldo Cruz Foundation, named the search for parasites in ancient material as “Paleoparasitology”, which means the study of parasites found in archaeological or paleontological material.

PREVIOUSLY Armand Ruffer was the first to record parasite eggs in mummified tissues of an Egyptian mummy (Ruffer 1910); Szidat (1944), Callen and Cameron (1955, 1960), Pike (1967), Fry and Moore (1969), Jones (1982), and others found parasite eggs in the intestinal contents of human mummified bodies or in coprolites

Dr. Luiz Fernando Ferreira

Araujo A 1980. [A contribution to the study of helminth eggs found in archaeological material, Brazil]. Master Thesis, Oswaldo Cruz Foundation.

Reinhard K 1985. Recovery of helminths from prehistoric feces: the cultural ecology of ancient parasitism. Master Thesis, Northern Arizona University.

Bouchet F 1995. Recovery of helminth eggs from archeological excavations of the Grand Louvre (Paris, France). Journal of Parasitology 81: 785-787.

Intestinal helminth eggs are commonly found in human coprolites

Karl Reinhard, diet and parasitism in Antelope Cave, USA, 1985

Coprolites can be preserved by desiccation or mineralized.

Coprolites are the most common source for intestinal helminths. Coprolites can be found isolated inside archaeological layers or agglomerated in latrines or cesspits (Bouchet et al. 2003).

However, intestinal contents of mummified bodies (Ferreira et al. 1980), sediments collected from the pelvic girdle of skeletons (Fugassa et al. 2005), or even the contents of discarded objects used to preserve the death (Harter et al. 2003) are recommended to be searched for parasite remains.

Morphological patterns help to establish the zoological origin of the coprolites found in each archaeological regionMorphology, food remains, and specific parasites also help to the diagnosis

Chame 2003. Mem Inst Oswaldo Cruz 98 suppl 1.

Parasites are considered as probes of ancient human migrations

Intestinal helminths, such as hookworms (Ancylostoma duodenale and Necatoramericanus), Trichuris trichiura, Ascarislumbricoides, Enterobius vermicularis, Strongyloides stercoralis were originated as human parasites in the Old World

They were found in organic remains in Old World archaeological sites

However, they were also found in organic remains collected in New World archaeological sites

Paleoparasitology methods are able to recover parasite remains, tracking parasites and their human hosts through every place to where they were dispersed

Araujo A, Reinhard K, Ferreria LF, Gardner SL, 2008.

Araujo, A, Ferreira, LF, Reinhard, K, 2008Neotropical zooarchaeology and taphonomyPages 1-4A. Sebastián Muñoz, Mariana Mondini

Reinhard K, 2005. Ancestral Pueblo Pathoecology – PAMINSA, Rio de Janeiro, Brasil

Enterobius vermicularis life cycle does not have an obligatory passage on the soil.

Therefore, external environment conditions have minimum influence on the transmission dynamics of the parasite

Enterobius vermicularis has its origin in African ancestors, and the infection was dispersed by human migrations to other parts of the world

Infection by Enterobius vermicularis was dispersed all over the world, no matter environmental conditions human hosts were living

Enterobius vermicularis infection crossed the Bering Strait from Siberia to Alaska with the first migrants to the Americas

However, the cold climate of the Bering Land Bridge hampered transmission of other human helminths.

These helminths are called geohelminths. Their life cycle have an obligatory passage on the soil, needing especial humidity, pH, and temperature conditions able to maintain eggs or larvae alive near 220C positive.

Arctic conditions played the role of a “filter” for many parasite infections.

Therefore, many Old World human infections were lost during the crossing of prehistoric human migrants to people the Americas.

North and South America -Hookworm – 7,000 years

North and South America -Trichuris trichiura – 8,000 years BP

North and South America -Ascaris lumbricoides – 9,000 years BP

These parasites could not have crossed the Bering Land Bridge with human hosts

PCR techniques applied to coprolites confirmed microscopic diagnosis, and amplified geographic distribution in the past

Trichuris trichiura ancient distribution

Paleoparasitologyand

Paleogeography

Ascaris lumbricoides ancient distribution

Hookworms, Trichuris trichiura,Ascaris lumbricoides,also originated as human parasites in the Old World.

These intestinal parasites were dispersed to other parts of globe where climate conditions allowed the maintenance of their life cycle

Hookworms, paleoclimate, and very rapid migration of the Clovis people.

Alvaro Montenegro+, Renée Hetherington+, Adauto Araujo*, Luiz Fernando Ferreira*, Andrew Weaver+ and Michael Eby+.

+ School of Earth and Ocean Sciences, University of Victoria, Victoria, BC, Canada.

*Escola Nacional de Saude Publica-Fiocruz, Rio de Janeiro, RJ, Brazil

Current Anthropology, Feb 2006

We proposed prehistoric transpacific contacts to explain the introduction of these intestinal helminths in the New World (Araujo et al. 1981, Ferreira et al. 1980, 1983, Ferreira & Araujo 1996, Reinhard et al. 2001, Faulkner & Patton 2001)

Intestinal helminth prevalence rates varied according to subsistence strategies as revealed by paleoparasitological data

North and South American Paleoindian groups subsisted as hunter-gatherers, living in medium/small groups

Later, in some regions of the Americas other people began to live in villages and population reached an expressive number, favoring parasite transmission

Paleoparasitological record revealed prevalence rate differences among hunter-gatherer and agriculturalist groups

Karl Reinhard showed that Ancestral Pueblos had different prevalence rates for Enterobius vermicularis infection comparing groups that lived on the Plateau and in the buildings inside the rock-shelters.

Grand Canyon Pueblos, Arizona, USA

In the Atacama desert of South American Pacific coast, Trichuris trichiura infectionwas found to be more prevalent among agriculturalists than in hunter-gatherer groups (Ferreira et al. 1984)

Atacama, Chile

Epidemiological transitions occurred along different moments during pre-Columbian times

Prevalence rates of intestinal helminth infections should have been varied among prehistoric American ancient populations

Population densities, combined with life strategies favored or hampered intestinal helminth transmission, according with their life strategies Machu Picchu, Peru

Le Bailly M, Leuzinger U, Schlichtherle H, Bouchet F. Diphyllobothrium: Neolithic parasite? J Parasitol.91(4): 957-959, 2005.

Le Bailly M, Bouchet F. Ancient dicrocoeliosis: Occurrence, distribution and migration. Acta Trop. Apr 2 [Epub ahead of print], 2010.

da Rocha GC, Harter-Lailheugue S, Le Bailly M, Ara√∫jo A, Ferreira LF, da Serra-Freire NM, Bouchet F. Paleoparasitological remains revealed by sevenhistoric contexts from "Place d'Armes", Namur, Belgium. Mem Inst Oswaldo Cruz 101 Suppl 2: 43-52, 2006.

Bouchet F, Harter S, Le Bailly M. The state of the art of paleoparasitological research in the Old World. Review. Mem Inst Oswaldo Cruz 98 Suppl 1: 95-101, 2003.

Bouchet F. Intestinal capillariasis in neolithic inhabitants of Chalain (Jura, France). The Lancet 349: 256 1997.

In contrast, paleoparasitological data pointed to New World low prevalence of intestinal helminths in most archaeological sites, especially of Ascaris

lumbricoides and Trichuris trichiura

Months after departing from Europe Portuguese and Spanish sailors described the New World as a Paradise, with healthy and happy people living without problems and no disease affecting them.

A prejudice appeared by the middle of the 19th century in Brazil attributing to African people the introduction of almost all transmissible diseases prevalent in

the country

J.B. Debret, slave market, Rio de Janeiro, 1816-1828

Paleoparasitological data showed that this was not true

Martin Fugassa, at the University of Mar del Plata, Argentina, showed that ancient people that lived in southern Patagonia was exposed to zoonosis

Intestinal helminths prevalence should be low because of the few eggs found in coprolites and skeleton sediments

Paleoepidemiological pattern changed when Europeans arrived

Paleoparasitological results showed clearly the difference between the number of intestinal helminth eggs in coprolites from European origin and those of the ancient inhabitants of Patagonia

100 0 100 200 Kilometers

N

EW

S

Archaeological sites

Hunter-gatherer

groups

European

colonization

Sea coast, steppe,

and forest-steppe

ecotone

Shell-midden, caves,

rock-shelthers, and

other burial sitesSouthern South America

Southern Patagonia SamplesTemporal location:

Pleistocene transition (10,600-9,000 years BP)Holocene (8,000 years-present)European contact (1520-1931 AD)

Origin:Sediments

skeleton remainsshell-middensoil occupied by ancient human groups

Coprolites

Ascaris lumbricoides

Trichuris trichiura

Filipe A. Carvalho-Costa, Adriano Gomes Silva, Alberto H. de Souza, Carlos J. de C. Moreira, Daniela L. de Souza, Joanna G. Valverde, Lauren H. Jaeger, Patrícia P. Martins, Viviane F. de Meneses, Adauto Araújo, Márcio N. Bóia. Pseudoparasitism by Calodium hepaticum (syn.Capillaria hepatica; Hepaticola hepatica) in theNegro River, Brazilian Amazon. Transactions of the Royal Society of Tropical Medicine and Hygiene 103(10):1071-1073, 2009.

Martín H Fugassa, Verónica Taglioretti, Marcelo LC Gonçalves, Adauto Araújo, Norma H Sardella, Guillermo M Denegri Capillaria spp. eggs in Patagonian archaeological sites: statistical analysis of morphometric data. Memorias do Instituto Oswaldo Cruz 103(1): 104-105, 2008.online | memorias.ioc.fiocruz.br

Dolichotis patagonum

Tapirus terrestris

Hunter-gatherers in the northeastern Brazil occupied the semiarid region called “caatinga”. In the archaeological region of National Park of Serra da Capivara Ascaris lumbricoides, Trichuris trichiura and hookworm eggs were found in human coprolites dated up to 7,230 years BP.These intestinal parasites are of Old World origin.

Parasites of animals were also found in human coprolites, showing what people was having as food. For example, both false parasitism and true infections called zoonosis caused by raw infected meet ingestion, or by direct contact of infected animals, were identified by paleoparasitological analysis. Some intestinal parasite species of animals may infect humans, but others cannot established themselves and disappear after some days. They can be used to recover the kind of diet people was using.

Parapharyngodon(Oxyurid) sp. in human coprolites

Macrofossils: seeds, lizard nail, insect head, unidentified bonefragment (40X). Picture: Isabel Teixeira.

Martín H Fugassa, Karl J. Reinhard, Keith L Johnson, Mônica Vieira, and Adauto Araújo MACRACANTHORHYNCHUS SP. (ARCHIACANTHOCEPHALA) IN A HUMAN COPROLITE FROM ANTELOPE CAVE, MOJAVE COUNTY, ARIZONAThe Jornal of Parasitology (in press)

C14 date of cal 680-890 AD (Beta 257786)

Enterobius vermicularis

Macracanthorhynchus sp.

The paleoepidemiological transition after the contact included social, cultural, environmental and biological changes for Native Americans. They were forced to live crowded, favoring parasite transmission, as exemplified by paleoparasitology both in North and South American historical sites. Therefore, we propose that the changing burden of disease in a short period of time probably lead to clinical problems rarely experimented before, as suggested by the medical literature from the period after the European conquest.

Albany, New York, USA – colonial period

Olinda, Pernambuco, Brasil – colonial period

Conclusions:1. Paloeparasitological record showed that the most common helminth

intestinal infections were prevalent among New World prehistoric populations

2. Ancylostomids (hookworm), ascariasis (roundworm), enterobiasis(pinworm), and trichuriasis (whipworm) infection were introduced in the New World by prehistoric migrants at least 10,000 years before present by transpacific contacts

3. These intestinal helminth infections were transmitted among prehistoric populations both in North and South America

4. Parasites of animals also were prevalent among prehistoric New World populations, as evidenced by paleoparasitological record

5. African slave trade was not responsible for the introduction of the most common intestinal helminth infections

6. European colonization promoted conditions to increase helminthtransmission, both among Europeans and Native Americans

7. There was a strong epidemiological transition when Europeans arrived, changing epidemiological patterns so far existing in the New World

This presentation is dedicated to our friend Patrick Horne who published the first review of Parasitism in the New World (HORNE, P.D. A review of the evidence of human endoparasitism in the pre-Columbian New World through the study of coprolites. Journal of Archaeological Science, 12: 299-310, 1985).

V WORLD CONGRESS ON MUMMY STUDIESTORINO, ITALYSeptember 2-5 2004