Herbivores Coprolites from Chehrabad Salt Mine of Zanjan, Iran (Sassanid Era, 224-651 AD) Reveals Eggs of Strongylidae and Anoplocephalidae Helminths
-
Masoumeh MEIGOUNI
,
Mahsasadat MAKKI
,
Ali HANILOO
,
Zeynab ASKARI
,
Iraj MOBEDI
,
Saied Reza NADDAF
,
Nicole BOENKE
,
Thomas STOLLNER
,
Abolfazl AALI
,
Zahra HEIDARI
,
Gholamreza MOWLAVI
Abstract
Background: The ancient Chehrabad Salt mine, a well-known archaeological site in Iran, has recently received increasing interest from Iranian and international archeologists. Also, the biological remains from this site have provided valuable sources for studying the pathogenic agents of ancient times. This study aimed to identify the parasitic helminth eggs preserved in the herbivores coprolites.
Methods: From 2011 to 2015, we received three coprolites belonging to herbivorous animals recovered during excavations in Chehrabad Salt mine of Zanjan, Iran. The coprolites were dated back to the Sassanid era (224-651 AD) by using radiocarbon accelerator mass spectrometry (AMS) and archeological stratigraphy methods. Following rehydration of the specimens in a 0.5% trisodium phosphate solution, the suspensions were mounted in glycerin jelly on glass slides and examined by a light microscope with 100x and 400x magnifications.
Results: Two coprolites belonged to donkeys and one to an unknown herbivore species. The recovered eggs belonged to members of two helminths families, Strongylidae, and Anoplocephalidae. Also, within the two coprolites, some mites, presumably of the order Oribatida, were observed.
Conclusion: The presence of two different nematodes in the equids coprolites provide clues of the burden of helminths infection on working animal at the Sassanid time and demonstrates the appropriate preservation condition of biological remains in the ancient salt mine of Chehrabad as well.
1. Sianto L, Chame M, Silva CS et al. Animal hel-minths in human archaeological remains: a review of zoonoses in the past. Rev Inst Med Trop Sao Paulo. 2009;51(3):119-30.
2. Ayele G, Feseha G, Bojia E, Joe A. Prevalence of gastro-intestinal parasites of donkeys in Dugda Bora District, Ethiopia. Livestock Research for Rural Development. 2006; 18(10):14-21.
3. Bu Y, Niu H, Gasser R et al. Strongyloid nematodes in the caeca of donkeys in Henan Province, China. Acta Parasitologica. 2009;54(3):263-8.
4. Umur Ş, Acici M. A survey on helminth infections of equines in the Central Black Sea region, Turkey. Turk J Vet Anim Sci. 2009;33(5):373-8.
5. Morgan SJ, Stromberg PC, Storts RW et al. Histology and morphometry of Strongylus vulgaris-mediated equine mesenteric arteritis. J Comp Pathol. 1991;104(1):89-99.
6. Whitlock J, Leasure E. Studies upon Strongylus vudgaris. I. The incidence of Strongylus vulgaris in mid-continental North America and the reaction of the infested ceca. Am J Hyg. 1939;29(3):83-7.
7. Le Bailly M, Lepetz S, Samashev Z et al. Palaeoparasitological study of gastro-intestinal content in horses at a Scythian kurgan (3rd century BC) found in Kazakhstan. Anthropozoologica. 2008;43(2):69-75.
8. Dufour B, Hugot JP, Lepetz S, Le Bailly M. The horse pinworm (Oxyuris equi) in archaeology during the Holocene: Review of past records and new data. Infect Genet Evol. 2015;33:77-83.
9. Khan M, Roohi N, Rana M. Strongylosis in equines: a review. J Anim Plant Sci. 2015;25:1-9.
10. Shite A, Admassu B, Abere A. Large strongyle Parastes in Equine: A Review. Adv Biol Res. 2015;9(4):247-52.
11. Denegri G, Bernadina W, Perez-Serrano J et al. Anoplocephalid cestodes of veterinary and medical significance: a review. Folia Parasitol (Praha). 1998;45(1):1-8.
12. Nezamabadi M, Mashkour M, Aali A et al. Identification of Taenia sp. in a natural human mummy (third century BC) from the Chehrabad salt mine in Iran. J Parasitol. 2013;99(3):570-2.
13. Mowlavi G, Makki M, Mobedi I et al. Paleoparasitological findings from rodent coprolites dated at 500 CE Sassanid Era in archeological site of Chehrabad (Douzlakh), salt mine Northwestern Iran. Iran J Parasitol. 2014;9(2):188-93.
14. Mowlavi G, Makki M, Heidari Z et al. Macracanthorhynchus hirudinaceus eggs in canine coprolite from the Sasanian Era in Iran (4th/5th Century CE). IJP. 2015;10(2):245.
15. Aali A, Stöllner T. (Eds.). The archaeology of the salt miners. Interdisciplinary Research 2010–2014. Deutsches Bergbau-Museum;2015.
16. Aali A, Abar A, Boenke N, Pollard M, Rühli F, Stöllner T. Ancient salt mining and salt men: the interdisciplinary Chehrabad Douzlakh project in North-Western Iran. Antiquity. 2012;86(333).
17. Reinhard KJ, Confalonieri UE, Herrmann B et al. Recovery of parasite remains from coprolites and latrines: aspects of paleoparasitological technique. Homo. 1986;37(4):217-239.
18. Makki M, Dupouy-Camet J, Sajjadi SMS et al. First Paleoparasitological Report on the Animal Feces of Bronze Age Excavated from Shahr-e Sukhteh, Iran. Korean J Parasitol. 2017;55(2):197-201.
19. Soulsby EJL. Helminths, arthropods and protozoa of domesticated animals: Bailliere Tindall; 1982.
20. Kaufmann J. Parasitic infections of domestic animals: a diagnostic manual. Birkhäuser Basel. 1996.
21. Getachew M, Trawford A, Feseha G, Reid S. Gastrointestinal parasites of working donkeys of Ethiopia. Trop Anim Health Prod. 2010;42(1):27-33.
22. Matthee S, Krecek RC, Milne SA. Prevalence and biodiversity of helminth parasites in donkeys from South Africa. J Parasitol. 2000;86(4):756-62.
23. Tavassoli M, Yamchi JA, Hajipour N. A survey on the prevalence of strongyles species in working donkeys in North-West of Iran. J Parasit Dis. 2016;40(4):1210-2.
24. Eslami A, Kiai B. Identification of cyathostomes in equines in Iran. Iran J Vet Res 2007;8(1):45-57.
25. Bhagwant S. Human Bertiella studeri (family Anoplocephalidae) infection of probable Southeast Asian origin in Mauritian children and an adult. Am J Trop Med Hyg. 2004;70(2):225-8.
26. Adams A, Webb L. Two further cases of human infestation with Bertiella studeri (Blanchard, 1891) Stiles and Hassall, 1902, with some observations on the probable synonymy of the specimens previously recorded from man. Ann Trop Med Parasitol. 1933;27(3):471-5.
27. Sun X, Fang Q, Chen XZ et al. Bertiella studeri infection, China. Emerg Infect Dis. 2006;12(1):176
28. Borji H, Moosavi Z, Ahmadi F. Cranial Mesenteric Arterial Obstruction Due To Strongylus vulgaris Larvae in a Donkey (Equus asinus). Iran J Parasitol.2014;9(3):441-4.
29. Bendrey R. Animal paleopathology. Encyclopedia of Global Archaeology. 2014:258-65.
30. Ampbell AJ, Gasser RB, Chilton NB. Differences in a ribosomal DNA sequence of Strongylus species allows identification of single eggs. Int J Parasitol. 1995;25(3):59–65.
31. Gasser RB, Stevenson LA, Chilton NB, Nansen P, Bucknell DG, Beveridge I. Species markers for equine strongyles detected in intergenic rDNA by PCR-RFLP. Mol Cell Probes. 1996;10(5):371–8.
32. Hung GC, Gasser RB, Beveridge I, Chilton NB. Species-specific amplification by PCR of ribosomal DNA from some equine strongyles. Parasitology. 1999;119:69–80.
33. Zhang LP, Hu M, Chilton NB, Huby-Chilton F, Beveridge I, Gasser RB. Nucleotide alterations in the D3 domain of the large subunit of ribosomal DNA among 21 species of equine strongyle. Mol Cell Probes. 2007;21(2):111–5.
34. Andersen UV, Howe DK, Olsen SN, Nielsen MK. Recent advances in diagnosing pathogenic equine gastrointestinal helminths: the challenge of prepatent detection.Vet Parasitol. 2013;192(1-3):1-9.
35. Leles D, Araújo A, Ferreira LF, Vicente ACP, Iñiguez AM. Molecular paleoparasitological diagnosis of Ascaris sp. from coprolites: new scenery of ascariasis in pre-Columbian South America times. Mem Inst Oswaldo Cruz. 2008;103(1):106-108.
36. Iñiguez AM, Reinhard KJ, Araújo A, Ferreira LF, Vicente ACP. Enterobius vermicularis: ancient DNA from North and South American human coprolites. Mem Inst Oswaldo Cruz. 2003;98:67-69.
2. Ayele G, Feseha G, Bojia E, Joe A. Prevalence of gastro-intestinal parasites of donkeys in Dugda Bora District, Ethiopia. Livestock Research for Rural Development. 2006; 18(10):14-21.
3. Bu Y, Niu H, Gasser R et al. Strongyloid nematodes in the caeca of donkeys in Henan Province, China. Acta Parasitologica. 2009;54(3):263-8.
4. Umur Ş, Acici M. A survey on helminth infections of equines in the Central Black Sea region, Turkey. Turk J Vet Anim Sci. 2009;33(5):373-8.
5. Morgan SJ, Stromberg PC, Storts RW et al. Histology and morphometry of Strongylus vulgaris-mediated equine mesenteric arteritis. J Comp Pathol. 1991;104(1):89-99.
6. Whitlock J, Leasure E. Studies upon Strongylus vudgaris. I. The incidence of Strongylus vulgaris in mid-continental North America and the reaction of the infested ceca. Am J Hyg. 1939;29(3):83-7.
7. Le Bailly M, Lepetz S, Samashev Z et al. Palaeoparasitological study of gastro-intestinal content in horses at a Scythian kurgan (3rd century BC) found in Kazakhstan. Anthropozoologica. 2008;43(2):69-75.
8. Dufour B, Hugot JP, Lepetz S, Le Bailly M. The horse pinworm (Oxyuris equi) in archaeology during the Holocene: Review of past records and new data. Infect Genet Evol. 2015;33:77-83.
9. Khan M, Roohi N, Rana M. Strongylosis in equines: a review. J Anim Plant Sci. 2015;25:1-9.
10. Shite A, Admassu B, Abere A. Large strongyle Parastes in Equine: A Review. Adv Biol Res. 2015;9(4):247-52.
11. Denegri G, Bernadina W, Perez-Serrano J et al. Anoplocephalid cestodes of veterinary and medical significance: a review. Folia Parasitol (Praha). 1998;45(1):1-8.
12. Nezamabadi M, Mashkour M, Aali A et al. Identification of Taenia sp. in a natural human mummy (third century BC) from the Chehrabad salt mine in Iran. J Parasitol. 2013;99(3):570-2.
13. Mowlavi G, Makki M, Mobedi I et al. Paleoparasitological findings from rodent coprolites dated at 500 CE Sassanid Era in archeological site of Chehrabad (Douzlakh), salt mine Northwestern Iran. Iran J Parasitol. 2014;9(2):188-93.
14. Mowlavi G, Makki M, Heidari Z et al. Macracanthorhynchus hirudinaceus eggs in canine coprolite from the Sasanian Era in Iran (4th/5th Century CE). IJP. 2015;10(2):245.
15. Aali A, Stöllner T. (Eds.). The archaeology of the salt miners. Interdisciplinary Research 2010–2014. Deutsches Bergbau-Museum;2015.
16. Aali A, Abar A, Boenke N, Pollard M, Rühli F, Stöllner T. Ancient salt mining and salt men: the interdisciplinary Chehrabad Douzlakh project in North-Western Iran. Antiquity. 2012;86(333).
17. Reinhard KJ, Confalonieri UE, Herrmann B et al. Recovery of parasite remains from coprolites and latrines: aspects of paleoparasitological technique. Homo. 1986;37(4):217-239.
18. Makki M, Dupouy-Camet J, Sajjadi SMS et al. First Paleoparasitological Report on the Animal Feces of Bronze Age Excavated from Shahr-e Sukhteh, Iran. Korean J Parasitol. 2017;55(2):197-201.
19. Soulsby EJL. Helminths, arthropods and protozoa of domesticated animals: Bailliere Tindall; 1982.
20. Kaufmann J. Parasitic infections of domestic animals: a diagnostic manual. Birkhäuser Basel. 1996.
21. Getachew M, Trawford A, Feseha G, Reid S. Gastrointestinal parasites of working donkeys of Ethiopia. Trop Anim Health Prod. 2010;42(1):27-33.
22. Matthee S, Krecek RC, Milne SA. Prevalence and biodiversity of helminth parasites in donkeys from South Africa. J Parasitol. 2000;86(4):756-62.
23. Tavassoli M, Yamchi JA, Hajipour N. A survey on the prevalence of strongyles species in working donkeys in North-West of Iran. J Parasit Dis. 2016;40(4):1210-2.
24. Eslami A, Kiai B. Identification of cyathostomes in equines in Iran. Iran J Vet Res 2007;8(1):45-57.
25. Bhagwant S. Human Bertiella studeri (family Anoplocephalidae) infection of probable Southeast Asian origin in Mauritian children and an adult. Am J Trop Med Hyg. 2004;70(2):225-8.
26. Adams A, Webb L. Two further cases of human infestation with Bertiella studeri (Blanchard, 1891) Stiles and Hassall, 1902, with some observations on the probable synonymy of the specimens previously recorded from man. Ann Trop Med Parasitol. 1933;27(3):471-5.
27. Sun X, Fang Q, Chen XZ et al. Bertiella studeri infection, China. Emerg Infect Dis. 2006;12(1):176
28. Borji H, Moosavi Z, Ahmadi F. Cranial Mesenteric Arterial Obstruction Due To Strongylus vulgaris Larvae in a Donkey (Equus asinus). Iran J Parasitol.2014;9(3):441-4.
29. Bendrey R. Animal paleopathology. Encyclopedia of Global Archaeology. 2014:258-65.
30. Ampbell AJ, Gasser RB, Chilton NB. Differences in a ribosomal DNA sequence of Strongylus species allows identification of single eggs. Int J Parasitol. 1995;25(3):59–65.
31. Gasser RB, Stevenson LA, Chilton NB, Nansen P, Bucknell DG, Beveridge I. Species markers for equine strongyles detected in intergenic rDNA by PCR-RFLP. Mol Cell Probes. 1996;10(5):371–8.
32. Hung GC, Gasser RB, Beveridge I, Chilton NB. Species-specific amplification by PCR of ribosomal DNA from some equine strongyles. Parasitology. 1999;119:69–80.
33. Zhang LP, Hu M, Chilton NB, Huby-Chilton F, Beveridge I, Gasser RB. Nucleotide alterations in the D3 domain of the large subunit of ribosomal DNA among 21 species of equine strongyle. Mol Cell Probes. 2007;21(2):111–5.
34. Andersen UV, Howe DK, Olsen SN, Nielsen MK. Recent advances in diagnosing pathogenic equine gastrointestinal helminths: the challenge of prepatent detection.Vet Parasitol. 2013;192(1-3):1-9.
35. Leles D, Araújo A, Ferreira LF, Vicente ACP, Iñiguez AM. Molecular paleoparasitological diagnosis of Ascaris sp. from coprolites: new scenery of ascariasis in pre-Columbian South America times. Mem Inst Oswaldo Cruz. 2008;103(1):106-108.
36. Iñiguez AM, Reinhard KJ, Araújo A, Ferreira LF, Vicente ACP. Enterobius vermicularis: ancient DNA from North and South American human coprolites. Mem Inst Oswaldo Cruz. 2003;98:67-69.
| Files | ||
| Issue | Vol 15 No 1 (2020) | |
| Section | Original Article(s) | |
| DOI | https://doi.org/10.18502/ijpa.v15i1.2533 | |
| Keywords | ||
| Paleoparasitology Herbivores Strongyle Anoplocephalan Iran | ||
| Rights and permissions | |
|
This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License. |
How to Cite
1.
MEIGOUNI M, MAKKI M, HANILOO A, ASKARI Z, MOBEDI I, NADDAF SR, BOENKE N, STOLLNER T, AALI A, HEIDARI Z, MOWLAVI G. Herbivores Coprolites from Chehrabad Salt Mine of Zanjan, Iran (Sassanid Era, 224-651 AD) Reveals Eggs of Strongylidae and Anoplocephalidae Helminths. Iran J Parasitol. 2020;15(1):109-114.
