Abstract
Paleoparasitological investigation in the archeological site of the Caspian Sea littoral revealed the presence of human Dioctophyma renale infection, a ubiquitous kidney-residing helminth of mammals, during the Parthian Empire of Iran (247 BC–224 AD). This study reports the oldest human infection with giant kidney worm in the Middle East, mainly in an area where the infection is reported nowadays. The paucity of records throughout the literature suggests that the same species of parasite occurred with low frequency in the past, as well. The cemetery in the archeological site of Kiasar represented a unique opportunity of studying human and animal parasites of the Parthian Empire in Iran.
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All data generated or analyzed during this study are included in this published article. The original datasets are available upon request to the corresponding author.
References
Amaro AA, Greer T, Wilson D, Smrdelj M (2022) Giant red kidney worm (Dioctophyma renale) infection in puppies less than four months of age from northern Canada. J Parasitol 108(2):127–131
Beaver PC, Jung RC, Cupp EW (1984) Clinical parasitology. Lea & Febiger, Philadelphia
Beugnet F, Halos L, Guillot J (2018) Textbook of clinical parasitology in dogs and cats. Servet Publishing Zaragoza
Bizhani N et al (2017) Dicrocoelium egg identified in an ancient cemetery in Kiasar archeological site, Northern Iran, Dated Back 247 BC–224 AD. Iran J Public Health 46(6):792
Caye P, Aguiar ES, Andrades JD, Neves KR, Rondelli MC, Braga FD, Grecco FB, Kaiser JF, Rappeti JC (2020) Report of rare case of intense parasitism by 34 specimens of Dioctophyme renale in a dog. Rev Bras Parasitol Vet 29(4):e011820
Chauhan S, Kaval S, Tewari S (2016) Dioctophymiasis: a rare case report. J Clin Diag Res 10(2):DD01–DD02
Cox FE (2002) History of human parasitology. Clin Microbiol Rev 15(4):595–612
Faust EC, Russell PF, Jung RC (1970) Craig and Faust’s clinical parasitology (1970) Craig and Faust’s clinical parasitology. 8th Edition, Lawrence, Kansas
Eslahi AV et al (2021) Occurrence of Dioctophyma renale (Goeze, 1782) in road-killed canids of Iran and its public health implication. Vet Parasitol Reg Stud Reports 24:100568
Ferreira LF, Reinhard KJ, Araújo A (2014) Foundations of paleoparasitology. Editora Fiocruz, Rio de Janeiro
Flórez ÁA, Russo J, Uribe N (2018) First report of Dioctophyma renale (Nematoda, Dioctophymatidae) in Colombia. Biomedica 38(2):13–18
Fugassa MH, Olivera EAG, Petrigh RS (2013) First palaeoparasitological record of a dioctophymatid egg in an archaeological sample from Patagonia. Acta Trop 128(1):175–177
Greer T, Amaro AA, Wilson D, Smrdelj M (2021) Giant red kidney worm (Dioctophyma renale) screening and treatment protocol and aberrant worm migration in dogs from Ontario and Manitoba, Canada. J Parasitol 107(2):358–363
Hajialilo E, Mobedi I, Masoud J, Hasanpour H, Mowlavi G (2015) Dioctophyma renale in Vulpes vulpes from the Caspian Sea littoral of Iran. Iran J Public Health 44(5):698
Hanjani A, Sadighian A, Nikakhtar B, Arfaa F (1968) The first report of human infection with Dioctophyma renale in Iran. Trans R Soc Trop Med Hyg 62(5):647–648
Hüster-Plogmann H, Leuzinger U (1995) Fischerei und Fischreste in der jungsteinzeitlichen Seeufersiedlung in Arbon (TG). Archäol Der Schweiz 18(3):109–117
Ignjatovic I, Stojkovic I, Kutlesic C, Tasic S (2003) Infestation of the human kidney with Dioctophyma renale. Urol Int 70(1):70–73
Jaeger LH, Iñiguez AM (2014) Molecular paleoparasitological hybridization approach as effective tool for diagnosing human intestinal parasites from scarce archaeological remains. PLoS ONE 9(8):e105910
Le Bailly M, Leuzinger U, Bouchet F (2003) Dioctophymidae eggs in coprolites from neolithic site of Arbon-Bleiche 3 (Switzerland). J Parasitol 89(5):1073–1076
Ledger ML, Mitchell PD (2022) Evolutionary perspectives on human parasitic infection: from ancient parasites to modern medicine. Palaeopathology and Evolutionary Medicine: An Integrated Approach 204-221. Oxford University Press, Oxfrod
Ledger ML, Grimshaw E, Fairey M, Whelton HL, Bull ID, Ballantyne R, Knight M, Mitchell PD (2019) Intestinal parasites at the Late Bronze Age settlement of Must Farm, in the fens of East Anglia, UK (9th century BCE). Parasitology 146(12):1583–1594
Li G, Liu C, Li F, Zhou M, Liu X, Niu Y (2010) Fatal bilateral dioctophymatosis. J Parasitol 96(6):1152–1154
Mowlavi G et al (2014) Paleoparasitological findings from rodent coprolites dated at 500 CE Sassanid Era in archeological site of Chehrabad (Douzlakh), salt mine Northwestern Iran. Iran J Parasitol 9(2):188
Neafie R, Marty A, Wear D (2000) Pathology of infectious diseases, Vol 1: Helminthiases. Edited by W. Meyers, Armed Forced Institute of Pathology (AFIP), DC Washington
Norouzi R, Manochehri A, Hanifi M (2017) A case report of human infection with Dioctophyma renale from Iran. Urol J 14(2):3043–3045
Otranto D, Stevens JR, Brianti E, Dorchies P (2006) Human and livestock migrations: a history of bot fly biodiversity in the Mediterranean region. Trends Parasitol 22(5):209–213
Pedrassani D, Nascimento AA, André MR, Machado RZ (2017) Dioctophyme renale: prevalence and risk factors of parasitism in dogs of São Cristóvão district, Três Barras county, Santa Catarina State, Brazil. Rev Bras Parasitol Vet 9(26):39–46
Pedrassani D, Wendt H, Rennau EA, Pereira ST, Wendt SBT (2014) Dioctophyme renale Goeze, 1782 in a cat with a supernumerary kidney. Rev Bras Parasitol Vet 23:109–111
Ramyar M, Amiri TA, Momeni O, Ghasemi MJ, Zaheer ZUR (2020) Tourists’ perspective on ecotourism infrastructures in Mazandaran Province of Iran. J Humanit Soc Sci Stud 2(3):109–118
Sharifi M, Shirazi R, Mousavi Kouhpar SM, Mahfroozi A (2016) Identifying the settlement patterns of East Mazandaran during the Chalcolithic Period. Pazhohesh-Ha-Ye Bastanshenasi Iran (in Persian) 6(10):47–66
Sianto L et al (2009) Animal helminths in human archaeological remains: a review of zoonoses in the past. Rev Inst Med Trop Sao Paulo 51:119–130
Urano Z, Hasegawa H, Katsumata T, Toriyama K, Aoki Y (2001) Dioctophymatid nematode larva found from human skin with creeping eruption. J Parasitol 87(2):462–465
Yang F, Zhang W, Gong B, Yao L, Liu A, Ling H (2019) A human case of Dioctophyma renale (giant kidney worm) accompanied by renal cancer and a retrospective study of dioctophymiasis. Parasite 26:1–8
Acknowledgements
We would like to express our gratitude to the School of Public Health, Tehran University of Medical Sciences, Tehran, Iran, for the provided amenities. Also, we are grateful to all staff at the Vestmin archeological site for their kind collaboration.
Funding
This study was financially supported by the Center for Research of Endemic Parasites of Iran (CREPI), Tehran University of Medical Science, Tehran, Iran (Grant No., 23083).
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NB and FN conducted the parasitological examination of the samples and drafting the manuscript. GM conceived, designed, and oversaw the study. AMS and MFK conducted the archeological sampling and examinations. NP participated in laboratory and material preparation. MBR, DO, and JDP provided guidance for drafting the manuscript and interpretation of the results. SM prepared the graphical illustrations and participated in drafting the manuscript and descriptive issues. All authors read and approved the final manuscript.
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Bizhani, N., Najafi, F., Rokni, M.B. et al. Tracking the existence of Dioctophyma renale in Parthian Empire of Iran (247 BC–224 AD). Parasitol Res 122, 413–418 (2023). https://doi.org/10.1007/s00436-022-07735-w
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DOI: https://doi.org/10.1007/s00436-022-07735-w