Molecular Identification of Falciparum Malaria and Human Tuberculosis Co-Infections in Mummies from the Fayum Depression (Lower Egypt)
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Due to the presence of the lake Quarun and to the particular nature of its irrigation system, it has been speculated that the Fayum, a large depression 80 kilometers south-west of modern Cairo, was exposed to the hazards of malaria in historic times. Similarly, it has been speculated that, in the same area, also human tuberculosis might have been far more widespread in the antiquity than in its recent past. If these hypotheses were confirmed, it would imply that frequent cases of co-infection between the two pathogens might have occurred in ancient populations. To substantiate those speculations, molecular analyses were carried out on sixteen mummified heads recovered from the necropolis of Abusir el Meleq (Fayum) dating from the 3(rd) Intermediate Period (1064-656 BC) to the Roman Period (30 BC-300 AD). Soft tissue biopsies were used for DNA extractions and PCR amplifications using well-suited protocols. A partial 196-bp fragment of Plasmodium falciparum apical membrane antigen 1 gene and a 123-bp fragment of the Mycobacterium tuberculosis complex insertion sequence IS6110 were amplified and sequenced in six and five of the sixteen specimens, respectively. A 100% concordance rates between our sequences and those of P. falciparum and M. tuberculosis complex ones were obtained. Lastly, concomitant PCR amplification of P. falciparum and M. tuberculosis complex DNA specific fragments was obtained in four mummies, three of which are (14)C dated to the Late and Graeco-Roman Periods. Our data confirm that the hydrography of Fayum was extremely conducive to the spread of malaria. They also support the notion that the agricultural boom and dense crowding occurred in this region, especially under the Ptolemies, highly increased the probability for the manifestation and spread of tuberculosis. Here we extend back-wards to ca. 800 BC new evidence for malaria tropica and human tuberculosis co-occurrence in ancient Lower Egypt.
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According to radiocarbon dates, the samples can be grouped into three time periods: Pre-Ptolemaic (New Kingdom, Third Intermediate Period and Late Period), Ptolemaic and Roman Period.
“According to the radiocarbon dates (Supplementary Data 1, see also ref. 18), the samples can be grouped into three time periods: Pre-Ptolemaic (New Kingdom, Third Intermediate Period and Late Period), Ptolemaic and Roman Period.”
From Ancient Egyptian mummy genomes suggest an increase of Sub-Saharan African ancestry in post-Roman periods (2017) · cites this paper as [18]
Table 1 (Introduction; page unavailable) gives radiocarbon dates for mummies assigned to the Third Intermediate, Late, Ptolemaic and Roman periods. It does not date any of its samples to the New Kingdom or group samples into the three stated categories; the Materials and Methods instead describe this study’s samples as spanning the Third Intermediate to Roman periods. (LLM, conf=0.86)
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- [2]Murray CJL, Rosenfeld LC, Lim SS, Andrews KG, Foreman KJ, et al (2012) Global malaria mortality between 1980 and 2010: a systematic analysis. Lancet 379: 413– 431. 22305225
- [4]Wiwanitkit V (2006) Co-infection between tuberculosis and malaria: a consideration on interaction of molecules and pathogenesis. J Vect Borne Dis 43: 195– 197. 17175706
- [5]Boraschi D, Alemayehu MA, Asella P, Chiodi F, Chisi J, et al (2008) Immunity against HIV/AIDS, Malaria and Tuberculosis during Co-Infections with Neglected Tropical Diseases. Recommendations for the European Union Research Priorities. PloS Negl Trop Dis 2(6): e255 doi: 10.1371/journal.pntd.0000255. 18575596 PMC2427178 · DOI
- [6]Bianucci R, Mattutino G, Lallo R, Charlier P, Jouin-Spriet H, et al (2008) Immunological evidence of Plasmodium falciparum Infection in a Child Mummy from the Early Dynastic Period. Journal of Archaeological Science 35: 1880– 1885.
- [7]Nerlich AG, Haas CJ, Zink A, Szeimies U, Hagedorn HG (1997) Molecular evidence for tuberculosis in an ancient Egyptian mummy. Lancet 350: 1404. 9365482
- [8]Crubezy E, Ludes B, Poveda JD, Clayton J, Crouau-Roy B, et al (1998) Identification of Mycobacterium DNA in an Egyptian Pott’s disease of 5,400 years old. C R Acad Sci III. 321: 941– 951. 9879471
- [9]Nerlich AG, Zink A, Hagedon H, Szeimies U, Weyss C (2000) Anthropological and paleopathological analysis of the human remains from three „Tombs of the Nobles“ of the necropolis of Thebes-West, Upper Egypt. Anthropol. Anz. 58(4): 321– 343. 11190927
- [10]Zink AR, Haas CJ, Reischl U, Szeimies U, Nerlich AG (2001) Molecular analysis of skeletal tuberculosis in an ancient Egyptian population. J Med Microbiol 50: 355– 366. 11289521
- [11]Zink AR, Grabner W, Reischl U, Wolf H, Nerlich AG (2003a) Molecular study on human tuberculosis on three geographically distinct and time delineated populations from Ancient Egypt. Epidemiol Infect 130: 239– 249. 12729192 PMC2869959
- [12]Zink AR, Sola Ch, Reischl U, Grabner W, Rastogu N, et al (2003b) Characterization of Mycobacterium tuberculosis Complex DNAs from Egyptian Mummies by Spoligotyping. J Clin Microbiol 41(1): 359– 367. 12517873 PMC149558
- [13]Donoghue HD, Lee OY-C, Minnikin DE, Besra GS, Taylor JH, et al (2010) Tuberculosis in Dr Granville’s mummy: a molecular re-examination of the earliest known Egyptian mummy to be scientifically examined and given a medical diagnosis. Proc. R. Soc. B. 277: 51– 56. PMC2842630 19793751
- [14]Nerlich AG, Schraut B, Dittrich S, Jelinek T, Zink AR (2008) Plasmodium falciparum in ancient Egypt. Emerg Infect Dis 14: 1317– 1319. 18680669 PMC2600410
- [15]Hawass Z, Gad YZ, Ismail S, Khairat R, Fathalla D, et al (2010) Ancestry and pathology in King Tutankhamun’s family. JAMA 303: 638– 647. 20159872
- [17]Bassiouny HK (2001) Bioenvironmental and metereological factors related tot he persistence of malaria in Fayoum Governatorate: a retrospective study. Eastern Mediterranean Health Journal 7(6): 895– 906. 15332730
- [18]Hassan FA (2010) Climate Change, Nile Floods and Riparia, in: Riparia Dans l’Empire Romain, Ella Ermon. BAR S2066, Oxford.
- [20]Koopman A, Kluiving S, Wendrich W, Holdaway S (2012) Late Quaternary Climate Change and Egypt’s Earliest Pre- Pharaonic Farmers, Fayum Basin, Egypt, in: W Bebermeier, R Hebenstreit, E Kaiser, J Krause (eds.), Landscape Archaeology, Proceedings of the International Conference Held in Berlin, 6th- 8th June 2012, 63–69.
- [22]Davoli P (2012) The Archaeology of Fayum, in: C Rigg (ed), The Oxford Handbook of Roman Egypt. Oxford Hanbooks Online, 153–169, doi: 10.1093/oxfordhb/9780199571451.001.0001. · DOI
- [23]Ikram S (2003) Death and Burial in Ancient Egypt. Longman (eds.), 207–222.
- [24]Keiser JM, De Castro C, Maltese MF, Bos R, Tanner M, et al (2005) Effects of irrigation and large dams in the burden of malaria on a global and regional scale. Am. J. Trop. Med, Hyg 72(4): 392– 406. 15827275
- [26]Scott CP, Kumar NY, Bishai WR, Manabe YC (2004) Report: Modulation of Mycobacterium tuberculosis Infection by Plasmodium in the Murine Model. Am. J. Trop. Med. Hyg. 70(2): 144– 148. 14993625
- [27]Hawkes M, Li X, Crockett M, Diassiti A, Liles WC, et al (2010) Malaria exacerbates experimental mycobacterial infection in vitro and in vivo. Microb Infect. 12: 864– 874. 20542132
- [28]Page KR, Jedlicka AE, Fakheri B, Noland GS, Kesavan AK, et al (2005) Mycobacterium-Induced potentiation of Type 1 Immune Responses and Protection against Malaria Are Host Specific. Infect. Immun. 73(12): 8369– 8380. PMC1307063 16299335
- [29]Enwere GC, Ota Mo, Obaro sK (1999) The host response in malaria and depression of defense against tuberculosis. Ann Trop. Med. Parastiol. 93: 669– 678. 10715693
- [30]Colombatti R, Pennazzato M, Bassani F, Vieira CS, Lourenço AA, et al.. (2011) Malaria prevention reduces in-hospital mortality among severely ill tuberculosis patients: a three- step intervention in Bissau, Guinea- Bissau. BMC Infectious Diseases 11(57) doi: 10.1186/1471-2334-11-57. PMC3056796 21366907 · DOI
- [31]Pahl WM (1982) Radiologische Untersuchungen an ägyptischen Mumien. Ein Beitrag zur modernen Mumienforschung unter Berücksichtigung ägyptologischer und medizinhistorischer Aspekte. Dissertation, Universität Tübingen.
- [35]McBride JS, Newbold CI, Anand R (1985) Polymorphism of a high molecular weight schizont antigen of the human malaria parasite Plasmodium falciparum. J Exp Med. 161: 160– 180. PMC2187544 2578540
- [36]Kiwanuka GN (2009) Genetic diversity in Plasmodium falciparum merozoite surface protein 1 and 2 coding genes and its implications in malaria epidemiology: a review of published studies from 1997–2007. J Vector Borne Dis 46: 1– 1. 19326702
- [37]Eisenach KD, Cave MD, Bates JH, Crawford JT (1990) Polymerase chain reaction amplification of a repetitive DNA sequence specific for Mycobacterium tuberculosis. J Infect Dis 161: 977– 981. 2109022
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Schuenemann, V. J., Peltzer, A., Welte, B., van Pelt, W. P., Molak, M., Wang, C.-C., Furtwängler, A., Urban, C., Reiter, E., Nieselt, K., et al. (2017) · Nature Communications · doi:10.1038/ncomms15694 · Cited by 201 · see citing works
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- Authors
- Lalremruata, A., Ball, M., Bianucci, R., Welte, B., Nerlich, A. G., Kun, J. F. J., & Pusch, C. M.
- Affiliations
- University of Tübingen (DE)
- University of Pisa (IT)
- Corresponding author
- Pusch, Carsten M.
- Venue
- PLoS ONE
- Publisher
- Public Library of Science (PLoS)
- Published
- 2013-04-02
- Volume
- 8
- Issue
- 4
- Pages
- e60307
- ISSN
- 1932-6203 (ISSN-L)
- PMC
- PMC3614933
- OpenAlex
- W2012782197
- Cited by
- 90
- References
- 0
- Citations by year
- 2026: 1 · 2025: 3 · 2024: 8 · 2023: 9 · 2022: 6 · 2021: 6 · 2020: 8 · 2019: 7 · 2018: 6 · 2017: 6 · 2016: 13 · 2015: 8 · 2014: 5 · 2013: 3
- FWCI
- 68.30
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- PLoS ONE (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, other-oa)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Funders
- Deutscher Akademischer Austauschdienst
- Topics
- Social Sciences › Arts and Humanities › Archeology › Paleopathology and ancient diseases
- Social Sciences › Arts and Humanities › History › History of Medicine Studies
- Social Sciences › Arts and Humanities › Archeology › Ancient Egypt and Archaeology
- Keywords
- Plasmodium falciparum, Mycobacterium tuberculosis complex, ancient mummies, Fayum Depression, IS6110 insertion sequence, ancient Egypt, malaria transmission, Ptolemaic period
- MeSH terms
- Adolescent, Adult, Antigens, Protozoan, Bacterial Proteins, Base Sequence, Child, Child, Preschool, Egypt, Female, Humans, Infant, Male, Membrane Proteins, Middle Aged, Molecular Sequence Data, Mummies, Mycobacterium tuberculosis, Plasmodium falciparum, Tuberculosis, Protozoan Proteins, Sequence Alignment, Malaria, Falciparum, Young Adult, Coinfection
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