Background: The Molavi street archeological site south of Tehran, Iran accidentally provided a unique opportunity for paleoparasitological studies in Iran. A female skeleton was unearthed and evaluated to be 7,000 years old. Soil samples were collected around the pelvic and sacrum bones.
Findings: Careful microscopic investigation of rehydrated soil samples revealed the presence of one Enterobius vermicularis egg attached to the skeleton sacral region.
Conclusion: The present finding likely represents the oldest evidence of a human pinworm infection in Asia

Dupouy Camet, Jean

Jelodar, Mohammad Esmaeili

Kia, Eshrat Beigom

Makki, Mahsasadat

Mobedi, Iraj

Mohebali, Mehdi

Mowlavi, Gholamreza

Najafi, Faezeh

Paknazhad, Niloofar

Rezaeian, Mostafa

Sarlak, Siamak

English

DigitalCommons@University of Nebraska

University of Nebraska - Lincoln DigitalCommons@University of Nebraska - Lincoln H. W. Manter Laboratory Library Materials 2016 Paleoparasitological Evidence of Pinworm (Enterobius vermicularis) Infection in a Female Adolescent Residing in Ancient Tehran (Iran) 7000 Years Ago Niloofar Paknazhad Tehran University of Medical Sciences Gholamreza Mowlavi Tehran University of Medical Sciences Jean Dupouy Camet Université Paris Descartes Mohammad Esmaeili Jelodar University of Tehran Iraj Mobedi Tehran University of Medical Sciences See next page for additional authors Follow this and additional works at: https://digitalcommons.unl.edu/manterlibrary  Part of the Archaeological Anthropology Commons, Biological and Physical Anthropology Commons, Parasitic Diseases Commons, and the Parasitology Commons Paknazhad, Niloofar; Mowlavi, Gholamreza; Dupouy Camet, Jean; Jelodar, Mohammad Esmaeili; Mobedi, Iraj; Makki, Mahsasadat; Kia, Eshrat Beigom; Rezaeian, Mostafa; Mohebali, Mehdi; Sarlak, Siamak; and Najafi, Faezeh, "Paleoparasitological Evidence of Pinworm (Enterobius vermicularis) Infection in a Female Adolescent Residing in Ancient Tehran (Iran) 7000 Years Ago" (2016). H. W. Manter Laboratory Library Materials. 28. https://digitalcommons.unl.edu/manterlibrary/28 This Article is brought to you for free and open access by DigitalCommons@University of Nebraska - Lincoln. It has been accepted for inclusion in H. W. Manter Laboratory Library Materials by an authorized administrator of DigitalCommons@University of Nebraska - Lincoln. Authors Niloofar Paknazhad, Gholamreza Mowlavi, Jean Dupouy Camet, Mohammad Esmaeili Jelodar, Iraj Mobedi, Mahsasadat Makki, Eshrat Beigom Kia, Mostafa Rezaeian, Mehdi Mohebali, Siamak Sarlak, and Faezeh Najafi This article is available at DigitalCommons@University of Nebraska - Lincoln: https://digitalcommons.unl.edu/manterlibrary/28 SHORT REPORT Open AccessPaleoparasitological evidence of pinworm(Enterobius vermicularis) infection in afemale adolescent residing in ancientTehran (Iran) 7000 years agoNiloofar Paknazhad1, Gholamreza Mowlavi1,2*, Jean Dupouy Camet3, Mohammad Esmaeili Jelodar4, Iraj Mobedi1,Mahsasadat Makki1, Eshrat Beigom Kia1, Mostafa Rezaeian1,2, Mehdi Mohebali1,2, Siamak Sarlak5and Faezeh Najafi1AbstractBackground: The Molavi street archeological site south of Tehran accidentally provided a unique opportunity forpaleoparasitological studies in Iran. A female skeleton was unearthed and evaluated to be 7000 years old. Soilsamples were collected around the pelvic and sacrum bones.Findings: Careful microscopic investigation of rehydrated soil samples revealed the presence of one Enterobiusvermicularis egg attached to the skeleton sacral region.Conclusion: The present finding likely represents the oldest evidence of a human pinworm infection in Asia.Keywords: Paleoparasitology, Enterobius vermicularis, Tehran, IranFindingsBackgroundBiological remains that are excavated from archeologicalsites are the main source of parasites that existed inancient times and paleoparasitologists, can take advan-tage of organic remains to identify ancient parasites ofhumans and animals. Therefore, coprolites, burial soilsamples and occasionally suspected parasitic objects [1]are always valuable material to paleoparasitologists.Excavation of a female skeleton at the “Molavi street”archeological site, has not only pushed back the presenceof humans living in Tehran to seven thousand years ago,but has also demonstrated the oldest occurrence of apinworm infection on the Asian continent. Formerstudies indicated that Enterobius vermicularis couldbe considered as the most ancient parasite of our humanancestors [2]. This exclusive obligate parasite of humans,directly transmitted from person to person, has a world-wide distribution and is very common in temperate andcool climate regions [3]. Evidence of pinworm infectionsin ancient populations has been demonstrated at differentarcheological sites on the American continent, Europeand Asia [4]. In Iran, eggs of E. vermicularis and Oxyurisequi have been found in soil samples collected from theChehrabad salt mine archeological site and dated back tobetween 1500–2500 years BC [5]. Moreover, eggs ofSyphacia obvelata a common oxyurid worm of mice andrats have also been diagnosed in rodent coprolites ex-cavated from the same archeological site [6].MethodsThe Molavi Street archeological site is located in thesouth of Tehran near the city’s Grand Bazaar. The sitebecame widely highlighted in newspapers and newsbroadcasts when, in 2014, a piece of ancient pottery wasfound in soil close to a civil water and sewage construc-tion project. Subsequent excavations, revealed a skeletonfound in a fetal position, four meters under the streetsurface. Thermoluminescence dating of pottery found* Correspondence: molavig@yahoo.com1Department of Parasitology and Mycology, School of Public Health, TehranUniversity of Medical Sciences, Tehran, Iran2Center for Research of Endemic Parasites of Iran (CREPI), Tehran Universityof Medical Sciences, Tehran, IranFull list of author information is available at the end of the article© 2016 Paknazhad et al. Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, andreproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link tothe Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver(http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.Paknazhad et al. Parasites & Vectors  (2016) 9:33 DOI 10.1186/s13071-016-1322-ynearby the skeleton provided two dates: 6870 ± 300 and6950 ± 280 BP [7]. Around 20 g of soil from the iliacfossa of pelvic bones, the coccyx, and apex regions ofthe sacrum were collected for paleoparasitological studies(Fig. 1a). For analysis, 10 g of the sample were rehydratedwith TSP solution, as previously described [6, 8]. From theentire rehydrated specimen 488 microscopic slides weremounted and examined [9].Ethical ApprovalAuthors declare that the procedures of sampling, studyingand reporting the current finding have followed in accord-ance with the ethical standards.Results & DiscussionOut of 488 microscopic slides that were examined onlyone egg similar to those of oxyurid worms was detected.At a first glance the apparent morphological features ofthe egg were undoubtedly those of E. vermicularis: theasymmetrical shape and the size of 30 × 60 μm that waswithin the usual size range (50 to 60 μm by 20 to30 μm), as reported [9, 10]. Few smaller microscopic ob-jects similar to cysts of protozoa and/or pollens werealso observed in the rehydrated material. In the absenceof reliable diagnostic methods all unidentified particleswere preserved for further studies using moleculartechniques. These findings from excavations at theMolavi street site have now extended the history of hu-man residence in Tehran back to the 5th millenniumBC, whereas previous findings in Gheytarieh Cemeteryin the northeast of Tehran estimated human presenceto only 1000 years BC.Identification of parasites in human and animal paleo-feces obtained from the archeological sites has shed lighton environmental conditions, levels of hygiene and manyother habits of humans from the past [11]. E. vermicu-laris is a directly transmitted parasitic nematode provok-ing anal or perianal pruritus in young children. Airborne transmission of E.vermicularis that is well toler-ated in communities nowadays [12] has been assumedto have developed in the distant past, when humanstended to settle in caves with limited air flow comparedto their wandering ancestors who lived in open air envir-onment [13]. The oldest record of a human infection isdated around 7837 BC in western Utah [14]. Severalstudies have also highlighted the controversial cause ofappendicitis due to E. vermicularis and its documentedrole in female urogenital tract disorders that should betaken into account by surgeons, or gynecologists per-forming laparoscopy [3, 15]. According to paleoparasito-logical findings of E.vermicularis eggs from differentparts of the world [16–18], the prevalence of infectionseems to be higher in primitive populations of Neolithicperiod, being lower in personal and environmental hy-giene level, than today's societies. Reports from differentparts of the modern world [14, 19, 20], emphasize thatthis worm is the most prevalent intestinal helminthic in-fection. As female Enterobius releases her eggs aroundthe perianal skin, stool examination is helpful in lessthan 5% of positive cases compared to the referenceGraham's scotch test [21]. In conclusion, human paleo-feces would not be appropriate samples for tracing en-terobiasis in ancient humans, except in heavy infectionssuch as the above mentioned oldest human enterobiasisFig. 1 The entire skeleton of the female adolescent excavated in Tehran archeological site, (a) showing the points of sampling (b) E.vermicularisegg retrieved from the collected sample (bar: 50 μm)Paknazhad et al. Parasites & Vectors  (2016) 9:33 Page 2 of 4record in Utah. However, due to more abundant para-site eggs near the anal region, the precise collectionof soil samples from the sacral foramina and aroundthe coccyx bones (Co1-Co4) could increase thechances of finding Oxyurid eggs (Fig. 1b). Distal phal-anxes of fingers, mostly the index, could also be an-other place for sampling, as Enterobius eggs havebeen found beneath the nails in 60 % of infectedcases reported in 1962 in Montreal, Canada [22]. Inthe present study, such samples could not be obtained,because of technical difficulties accessing the fingers anddue to restrictions of official regulations. In addition, theclinical consequences of ectopic enterobiasis, particularlyappendicitis [23, 24], generalized peritonitis [25], and fe-male urogenital disorders [26] might have seriously threat-ened the life of primitive families. Therefore, the impact ofenterobiasis on females and the well-being of children inpre-historic times should be re-evaluated throughout hu-man history. The present parasitological and archeologicalfinding at this burial has not only demonstrated the oldestpossible occurrence of a human pinworm infection in thispart of the world, but also has confirmed the human resi-dency in the 5th millennia BC in Tehran.Competing interestsThe authors declare that they have no competing interests.Authors’ contributionsNP: Carried out the paleoparasitological studies. Participated in laboratorydiagnosis as the MS student and attended the discussion groups. GM:Participated in paleoparasitology as supervisor and attended the discussiongroups. JDC: Acted as a Consultant throughout the entire stages of the studyand drafted the manuscript. MEEJ: Carried out the archeological excavation.Participated in archeological and anthropological data collections andinterpretations and drafted the manuscript. IM: Carried out paleoparasitologicalstudies: participated in diagnosis confirmation as an Iranian pioneer onHelminthology. MR: Carried out paleoparasitological studies: participated in sitevisit and in professional sampling and drafted the manuscript. MM: Carried outthe paleoparasitological studies. Participated in laboratory technique andattended the discussion groups. EBK: Conceived of the study, andparticipated in its design and coordination and helped to draft themanuscript. MM: Participated in the design of the study and performedthe comparative description and attended the discussion groups. SS:Carried out the archeological excavation. Participated in archeologicaland anthropological data collections and interpretations. FN: Carried outthe paleoparasitological studies. Participated in laboratory technique. Allauthors read and approved the final version of the manuscript.AcknowledgmentsThe Present study was conducted within a framework of collaborationbetween the Faculty of Letters and Humanities at Tehran University andTehran Province Water and Wastewater Company under the supervision ofthe Research Institute of Cultural Heritage and Tourism. The scientific effortof the Iranian Center for Archeological Research (ICAR) is also appreciated.We also gratefully acknowledge Mr. Behnam Ghanbari and Mr. SaeidZolghadr for their technical assistance. The assistance of Miss NegarBizhani during the entire study was highly appreciated. Special thanksalso to Dr. Gordon Langsley for the English revision of the manuscript.Author details1Department of Parasitology and Mycology, School of Public Health, TehranUniversity of Medical Sciences, Tehran, Iran. 2Center for Research of EndemicParasites of Iran (CREPI), Tehran University of Medical Sciences, Tehran, Iran.3Service de Parasitologie-Mycologie, Hôpital Cochin Assistance PubliqueHôpitaux de Paris, Université Paris Descartes, 27 Faubourg St Jacques, 75014Paris, France. 4Department of Archaeology Faculty of Letters and HumanitiesUniversity of Tehran, Tehran, Iran. 5Member of Iranian Center forArchaeological Research, Siye Tir Street, Imam Khomeini Avenue, Tehran, Iran.Received: 18 November 2015 Accepted: 19 January 2016References1. Mowlavi G, Kacki S, Dupouy-Camet J, Mobedi I, Makki M, Harandi MF, et al.Probable hepatic capillariosis and hydatidosis in an adolescent from the lateRoman period buried in Amiens (France). Parasite. 2014;21.2. Iñiguez AM, Reinhard KJ, Araújo A, Ferreira LF, Vicente ACP. Enterobiusvermicularis: ancient DNA from North and South American humancoprolites. Mem Inst Oswaldo Cruz. 2003;98:67–9.3. Ariyarathenam A, Nachimuthu S, Tang T, Courtney E, Harris S, Harris A.Enterobius vermicularis infestation of the appendix and management at thetime of laparoscopic appendicectomy: Case series and literature review. IntJ Surg. 2010;8(6):466–9.4. Gonçalves MLC, Araújo A, Ferreira LF. Human intestinal parasites in thepast: new findings and a review. Mem Inst Oswaldo Cruz. 2003;98:103–18.5. Nezamabadi M, Aali A, Stöllner T, Mashkour M, Le Bailly M. Paleoparasitologicalanalysis of samples from the Chehrabad salt mine (Northwestern Iran).International Journal of Paleopathology. 2013;3(3):229–33.6. 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Paleoparasitological Evidence of Pinworm (\u3ci\u3eEnterobius vermicularis\u3c/i\u3e) Infection in a Female Adolescent Residing in Ancient Tehran (Iran) 7000 Years Ago

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Paleoparasitological Evidence of Pinworm (\u3ci\u3eEnterobius vermicularis\u3c/i\u3e) Infection in a Female Adolescent Residing in Ancient Tehran (Iran) 7000 Years Ago

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