Year : 2015 | Volume
: 8 | Issue : 1 | Page : 1--3
The amazing adventure of parasitologists chasing mummies
Noha A Elleboudy
Department of Parasitology, Faculty of Medicine, Ain-Shams University, Cairo, Egypt
Noha A Elleboudy
Department of Parasitology, Faculty of Medicine, Ain-Shams University, Cairo 11351
|How to cite this article:|
Elleboudy NA. The amazing adventure of parasitologists chasing mummies.Parasitol United J 2015;8:1-3
|How to cite this URL:|
Elleboudy NA. The amazing adventure of parasitologists chasing mummies. Parasitol United J [serial online] 2015 [cited 2023 Mar 26 ];8:1-3
Available from: http://www.new.puj.eg.net/text.asp?2015/8/1/1/163401
Studying the life of extinct populations has always been an attractive field of science that drew the attention of different specialties all over the world; among these specialists are the parasitology scientists. Paleoparasitology was introduced as the study of ancient parasites with special emphasis on parasitism interaction with the host or the vector. Archeological sites provide vast amounts of material to support these investigations  . Paleoparasitology, introduced by the late 70s, is a relatively recent science  that delves into the historical communal perspectives and epidemiological information on parasitic diseases in ancient times  .
When paleoparasitology started?
The early discovery of Schistosoma haematobium eggs in the kidney of a 3200-year-old Egyptian mummy by Ruffer in 1910  drew special attention to paleoparasitology at a time when research work originating from Egypt was scarce  .
Why study paleoparasitology?
Since its emergence, paleoparasitology has added experiential data on infections, clinical disease conditions, and their epidemiological patterns among populations that have already vanished from both the Old and the New worlds  . Besides, it provides data on the evolution and the phylogenetic diversification of parasites and changes in virulence and pathogenicity  . It also helps in understanding the occupation of territories and in retracing the migratory paths of prehistoric populations leading to the spread of parasites  .
What can paleoparasitology tell?
The study of ancient parasites recovered paleontological data that contributed to the study of pathways of migration of ancient civilizations. Such movements allowed the dispersal of many parasites from the Old world to the New world. Paleoparasitology also supplied information that threw light on the social background of these diseases. Notably, hunters were found to be associated with zoonotic infections, and agricultural populations were more exposed to specific parasites. In prehistoric agricultural villages, levels of parasitism were found to be dependent on the structures of housing and the sanitation patterns  .
Interestingly, some current parasitic human infections were recorded from the prehistoric era, indicating that the parasites involved could maintain their life cycles over time in new environments. In contrast, some parasites that existed during the history of human evolution were lost over time  . In one example, the relation between parasitism and anemia was confirmed, linking the parasite prevalence in coprolites with bone lesion in mummified skeletons  .
Where to find samples?
Organic remains comprise the foremost source for paleoparasitological studies. These generally constitute coprolites, latrine and soil sediments, mummified tissues, hairs, and many other organic remains. Coprolites are the most important source, but latrine and soil sediments are also common sites for supplying research material  . Identification of the animal origin of coprolites found in each archaeological region depends on its morphological pattern, the included food remains, and specifically the parasites found in the coprolite  . It was noted that these samples should be handled with significant caution to avoid contamination of their ancient DNA (aDNA) content  .
How to perform paleoparasitological examination?
To analyze coprolites, the trisodium phosphate rehydration technique was introduced successfully. This reconstitution technique allowed the possible preservation of both shells of eggs and morphological features of larvae such as the esophagus and the intestine  . The common techniques to examine stool samples were applied after hydration, light microscopic examination being the main tool applied after different concentration techniques of stool and soil samples  . Electron microscopy was also used for structure identification of different parasites' eggs  .
As protozoan parasites cannot withstand desiccation, special techniques are required for their identification. These include immunofluorescence stains for Giardia lamblia cysts and antigen detection for Entamoeba histolytica, Cryptosporidium, and G. lamblia  . Histopathological examinations of mummies revealed Chagas' disease  and cutaneous leishmaniasis  . Other more up-to-date techniques such as neutron imaging, X-ray, synchrotron computed tomography, nuclear MRI, and Raman spectroscopy were used successfully  . In addition, molecular paleoparasitology studies of aDNA recovered from archaeological material or museum specimens opened new insights in paleoparasitology  . By the isolation of aDNA, it was possible to characterize Trichuris trichiura, Enterobius vermicularis, and Ascaris lumbricoides , molecularly from the archaeological material, and recently, Leishmania tarentolae was reported from a Brazilian mummy  .
The recovery of parasites' genomes from paleontological samples and comparing them with those from recent ones encourage the study of genome evolution through time. Using molecular paleoparasitological techniques, the phylogeny, the origin, the dispersion, the virulence, and the pathogenicity of past existing parasites will be understood more clearly  . However, obstacles that need to be overcome include the breaking of tissues into small fragments for amplification, deamination of nucleotides, adverse characteristics of aDNA such as amino-acid racemization, poorly characterized PCR inhibitors of aDNA, and the need for special DNA polymerases  .
Molecular paleoparasitology protocols constitute one-step conventional PCR, nested and heminested PCR, and the least used is real-time PCR  . Amplified fragments are cloned before sequencing by capillary automatic sequencers, and the possibility of contamination may be overcome by a nested PCR (suicide PCR) in which both the target DNA fragment and the primers are used only once  . Also, aDNA hybridization technique was introduced as a confirming and complementing alternative tool to PCR  .
The rise of metagenomics in the late 90s permitted the recovery of multiple genomes and the sequencing of thousands of organisms in parallel in a single run. Still, so far, there are few reports on the detection of parasitic infections, except for a primary trial to sequence Plasmodium and Toxoplasma in genetic materials from Egyptian mummies  . The application of random shotgun metagenomics shows the potential for the recovery of parasites' sequences from ancient material and museum samples, but still requires more input to reach a satisfactory parasitic metagenomics result , .
Besides PCR technology and immunological analyses, newer progresses have been made with laser confocal microscopy, which has proven its efficacy in characterizing lesions caused by ancient parasites. Also, there is environmental scanning electron microscopy, which requires a simple preparation of specimens for parasite studies from delicate mummy samples  . Being noninvasive, paleoradiological examination studies of mummies have proven invaluable and have contributed significantly to update the information. Several such research projects are still in progress  . There is the Schistosomiasis Project in collaboration between the University of Manchester and the Egyptian Ministry of Health based on immunocytochemical survey techniques  , and the University of Pisa project named 'Anubis' carried out on 46 Egyptian mummies in Italian museums  . In the latter project, a case of cysticercosis was documented.
Which parasites were recovered successfully?
Paleoparasitological findings recovered from organic remains in both Old-world and New-world archaeological sites consist mostly of eggs, less frequently larvae of intestinal parasites, or chitin exoskeletons of ectoparasites  , whereas those of protozoan parasites are rare. However, their antigens can remain recognizable for a long time  .
Conversation with Egyptian mummies
Numerous Egyptian mummies are still being provided by excavation campaigns, and several of these have been transferred to museums abroad, presenting opportunities for more enlightening research in ancient Egyptian parasitology  . The study of mummies has drawn attention since 1994, as it is an important source for recovering coprolite material that may contain adult and larval stages of parasites as well as ectoparasites, aDNA, and other biological samples. Advances in paleoparasitology rely on the techniques used in the examination of the mummies study.
Egyptian mummies have provided evidence that parasitic diseases were, at that time, one of the most common health problems in ancient Egypt  . The study of mummies' has revealed several parasites such as the aDNA of Leishmania donovani  and both Schistosoma mansoni and S. haematobium  ; samples of the embalming jars' content showed Ascaris and Taenia eggs from Akhthetep's mastaba of Saqqara in 2001  . 'Ebers papyrus', which has mentioned several other parasites, and stressed on the ancient Egyptian familiarity with parasites, was discussed thoroughly by Azab in 2013  .
Interpreting the ecology of ancient parasitic diseases and the comprehensive study of the species diversity of protozoa, helminths, and arthropods may be accomplished by expanding paleoparasitology from coprolites and soils to target mummies  . Tissue bank samples of mummies can contribute to the study of the pattern and the development of parasitic diseases that occurred in ancient Egypt. Resolving the question of whether the genetic makeup of parasites has changed over thousands of years may help in interpreting their ecology and improving the historical preventive means of treatment for use in present times.
Conflicts of interest
There are no conflicts of interest.
|1||Seo M, Araujo A, Reinhard K, Chai JY, Shin DH. Paleoparasitological studies on mummies of the Joseon Dynasty, Korea. Korean J Parasitol 2014; 52:235-242.|
|2||Bartošová L, Ditrich O, Beneš J, Frolík J, Musil J. Paleoparasitological findings in medieval and early modern archaeological deposits from Hradební Street, Chrudim, Czech Republic. Interdisciplinaria Achaeologica. Natural Sciences in Archaeology 2011; 2:27-28.|
|3||Reinhard KJ, Araújo A. Archaeoparasitology. In: Pearsall D, editor. Encyclopedia of archaeology. 1st ed. New York: Elsevier, Academic Press; 2008;494-501.|
|4||Ruffer, MA. Note on the presence of ′Bilharzia haematobia′ in Egyptian mummies of the twentieth dynasty [1250-1000 B.C.]. Br Med J 1910; 1:2616.|
|5||Faulkner CT, Reinhard KJ. A retrospective examination of paleoparasitology and its establishment in the Journal of Parasitology. J Parasitol 2014; 100:253-259.|
|6||Welsh EC. Parasitic nematodes in humans. Exploring the host-parasite dynamic through historical, biological, and public health evaluations of infection [MSc thesis], Kentucky. University of Louisville; 2012.|
|7||Araújo A, Jansen AM, Bouchet F, Reinhard K, Ferreira LF. Parasitism, the diversity of life, and paleoparasitology. Mem Inst Oswaldo Cruz 2003; 98: Suppl 1:5-11.|
|8||Fornaciari G, Gaeta R. Paleoparasitology of helminths. In: Bruschi F, editor. Helminth infections and their impact on global public health. ISBN: 978-3-7091-1781-1 (Print) 978-3-7091-1782-8 (Online). 1st ed. Heidelberg: Springer publications; 2014. 29-47.|
|9||Bouchet F, Harter S, Le Bailly M. The state of the art of paleoparasitological research in the Old World. Mem Inst Oswaldo Cruz 2003; 98: Suppl 1:95-101.|
|10||Araujo A, Reinhard K, Bastos OM, Costa LC, Pirmez C, Iñiguez A, et al. Paleoparasitology: perspectives with new techniques. Rev Inst Med Trop Sao Paulo 1998; 40:371-376.|
|11||Piojos PD, Precolombina ES. Paleoepidemiology of intestinal parasites and lice in pre-Columbian South America. Chungara Revista de Antropología Chilena 2011; 43:303-313.|
|12||Gonçalves ML, Araújo A, Ferreira LF. Human intestinal parasites in the past: new findings and a review. Mem Inst Oswaldo Cruz 2003; 98: Suppl 1:103-118.|
|13||Drancourt M, Raoult D. Molecular detection of past pathogens. In: Raoult D, Drancourt M, editors. Paleomicrobiology: past human infections. 1st ed. Heidelberg: Springer-Verlag; 2008. 55-58.|
|14||Shin DH, Lim DS, Choi KJ, Oh CS, Kim MJ, Lee IS et al. Scanning electron microscope study of ancient parasite eggs recovered from Korean mummies of the Joseon Dynasty. J Parasitol 2009; 95:137-145.|
|15||Araújo A, Jansen AM, Reinhard K, Ferreira LF. Paleoparasitology of Chagas disease - a review. Mem Inst Oswaldo Cruz 2009; 104: Suppl 1:9-16.|
|16||Lynnerup N, Lynnerup N, Gilbert MT, Djurhuus D, Melchior L, Lynnerup N, et al. Mummies. Am J Phys Anthropol 2007; Suppl 45:162-190.|
|17||Kefi R. Ancient DNA investigations. A review on their significance in different research fields. Int J Mod Anthropol 2011; 1:61-76.|
|18||Jaeger LH, Iniguez AM. Molecular paleoparasitological hybridization approach as effective tool for diagnosing human intestinal parasites from scarce archaeological remains. PLoS One 2014; 9:e105910. |
|19||Novo SP, Leles D, Bianucci R, Araujo A. Leishmania tarentolae molecular signatures in a 300 hundred-years-old human Brazilian mummy. Parasit Vectors 2015: 8:72. |
|20||Fournier PE, Raoult D. Suicide PCR on skin biopsy specimens for diagnosis of rickettsioses. J Clin Microbiol 2004; 42:3428-3434.|
|21||Khairat R, Ball M, Chang CC, Bianucci R, Nerlich AG, Trautmann M, et al. First insights into the metagenome of Egyptian mummies using next-generation sequencing. J Appl Genet 2013; 54:309-325.|
|22||Warnecke F, Hugenholtz P. Building on basic metagenomics with complementary technologies. Genome Biol 2007; 8:231.|
|23||Pallen MJ. Diagnostic metagenomics: potential applications to bacterial, viral and parasitic infections. Parasitology 2014; 141:1856-1862.|
|24||Shin DH, Oh CS, Kim MJ, Yoo DS, Lee IS. What could radiological study say about Korean mummies? ISBN 978-3-89937-163-5, Mannheim, Germany. Yearbook of Mummy Studies 2014; 2:125-131. |
|25||Giuffra VA, Pangoli DO, Cosmacini PA, Caramella DA, Silvano FL, Fornaciari GI et al. Paleopathological evaluation and radiological study of 46 Egyptian mummified specimens in Italian museums. EVO 2009; 32:121-155.|
|26||Panagiotakopulu E. Dipterous remains and archaeological interpretation. J Archaeol Sci 2004; 31:1675-1684.|
|27||Zink AR, Spigelman M, Schraut B, Greenblatt CL, Nerlich AG, Donoghue HD. Leishmaniasis in ancient Egypt and Upper nubia. Emerg Infect Dis 2006; 12:1616-1617. |
|28||Matheson CD, David R, Spigelman M, Donoghue HD. Molecular confirmation of Schistosoma and family relationship in two ancient Egyptian mummies. ISBN 978-3-89937-163-5, Mannheim, Germany. Yearbook of Mummy Studies 2014; 2:39-47. |
|29||Harter S, Le Bailly M, Janot F, Bouchet F. First paleoparasitological study of an embalming rejects jar found in Saqqara, Egypt. Mem Inst Oswaldo Cruz 2003; 98: Suppl 1:119-121.|
|30||An interview with Prof. Dr Magda Azab. Trop Parasitol 2013; 3:170-174. |
|31||Panagiotakopulu E, Buckland P. Environment, insects and the archaeology of Egypt. In: Ikram S, Dodson A, editor. Beyond the horizon: studies in Egyptian Art. Vol. 2. Cairo: Publications of the Supreme Council of Antiquities; 2010;347-361.|