Opisthorchiasis in infant remains from the medieval Zeleniy Yar burial ground of XII-XIII centuries AD
Identifieur interne : 000021 ( Pmc/Corpus ); précédent : 000020; suivant : 000022Opisthorchiasis in infant remains from the medieval Zeleniy Yar burial ground of XII-XIII centuries AD
Auteurs : Sergey Mikhailovich Slepchenko ; Alexander Vasilevich Gusev ; Sergey Nikolaevich Ivanov ; Evgenia Olegovna SvyatovaSource :
- Memórias do Instituto Oswaldo Cruz [ 0074-0276 ] ; 2015.
Abstract
We present a paleoparasitological analysis of the medieval Zeleniy Yar burial ground
of the XII-XII centuries AD located in the northern part of Western Siberia. Parasite
eggs, identified as eggs of
Url:
DOI: 10.1590/0074-02760150156
PubMed: 26602874
PubMed Central: 4708016
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PMC:4708016Le document en format XML
<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">Opisthorchiasis in infant remains from the medieval Zeleniy Yar burial
ground of XII-XIII centuries AD</title>
<author><name sortKey="Slepchenko, Sergey Mikhailovich" sort="Slepchenko, Sergey Mikhailovich" uniqKey="Slepchenko S" first="Sergey Mikhailovich" last="Slepchenko">Sergey Mikhailovich Slepchenko</name>
<affiliation><nlm:aff id="aff1">Siberian Branch of the Russian Academy of Sciences, Institute for Problems of the Development of the North, Tyumen, Siberia, Russia</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Gusev, Alexander Vasilevich" sort="Gusev, Alexander Vasilevich" uniqKey="Gusev A" first="Alexander Vasilevich" last="Gusev">Alexander Vasilevich Gusev</name>
<affiliation><nlm:aff id="aff2">YaNAO Arctic Research Center, Archeology Department, Archeology and Ethnology Sector, Salekhard, YaNAO, Russia</nlm:aff>
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<author><name sortKey="Ivanov, Sergey Nikolaevich" sort="Ivanov, Sergey Nikolaevich" uniqKey="Ivanov S" first="Sergey Nikolaevich" last="Ivanov">Sergey Nikolaevich Ivanov</name>
<affiliation><nlm:aff id="aff1">Siberian Branch of the Russian Academy of Sciences, Institute for Problems of the Development of the North, Tyumen, Siberia, Russia</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Svyatova, Evgenia Olegovna" sort="Svyatova, Evgenia Olegovna" uniqKey="Svyatova E" first="Evgenia Olegovna" last="Svyatova">Evgenia Olegovna Svyatova</name>
<affiliation><nlm:aff id="aff3">Institution of Culture of Sverdlovsk Region, Center for Protection and Use of Monuments of History and Culture of Sverdlovsk Region, Scientific and Production Center, Ekaterinburg, Urais, Russia</nlm:aff>
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<sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Opisthorchiasis in infant remains from the medieval Zeleniy Yar burial
ground of XII-XIII centuries AD</title>
<author><name sortKey="Slepchenko, Sergey Mikhailovich" sort="Slepchenko, Sergey Mikhailovich" uniqKey="Slepchenko S" first="Sergey Mikhailovich" last="Slepchenko">Sergey Mikhailovich Slepchenko</name>
<affiliation><nlm:aff id="aff1">Siberian Branch of the Russian Academy of Sciences, Institute for Problems of the Development of the North, Tyumen, Siberia, Russia</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Gusev, Alexander Vasilevich" sort="Gusev, Alexander Vasilevich" uniqKey="Gusev A" first="Alexander Vasilevich" last="Gusev">Alexander Vasilevich Gusev</name>
<affiliation><nlm:aff id="aff2">YaNAO Arctic Research Center, Archeology Department, Archeology and Ethnology Sector, Salekhard, YaNAO, Russia</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Ivanov, Sergey Nikolaevich" sort="Ivanov, Sergey Nikolaevich" uniqKey="Ivanov S" first="Sergey Nikolaevich" last="Ivanov">Sergey Nikolaevich Ivanov</name>
<affiliation><nlm:aff id="aff1">Siberian Branch of the Russian Academy of Sciences, Institute for Problems of the Development of the North, Tyumen, Siberia, Russia</nlm:aff>
</affiliation>
</author>
<author><name sortKey="Svyatova, Evgenia Olegovna" sort="Svyatova, Evgenia Olegovna" uniqKey="Svyatova E" first="Evgenia Olegovna" last="Svyatova">Evgenia Olegovna Svyatova</name>
<affiliation><nlm:aff id="aff3">Institution of Culture of Sverdlovsk Region, Center for Protection and Use of Monuments of History and Culture of Sverdlovsk Region, Scientific and Production Center, Ekaterinburg, Urais, Russia</nlm:aff>
</affiliation>
</author>
</analytic>
<series><title level="j">Memórias do Instituto Oswaldo Cruz</title>
<idno type="ISSN">0074-0276</idno>
<idno type="eISSN">1678-8060</idno>
<imprint><date when="2015">2015</date>
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<front><div type="abstract" xml:lang="en"><p>We present a paleoparasitological analysis of the medieval Zeleniy Yar burial ground
of the XII-XII centuries AD located in the northern part of Western Siberia. Parasite
eggs, identified as eggs of <italic>Opisthorchis felineus</italic>
, were found in the
samples from the pelvic area of a one year old infant buried at the site. Presence of
these eggs in the soil samples from the infant’s abdomen suggests that he/she was
infected with opisthorchiasis and imply consumption of undercooked fish. Ethnographic
records collected among the population of the northern part of Western Siberia reveal
numerous cases of feeding raw fish to their children. Zeleniy Yar case of
opisthorchiasis suggests that this dietary custom has persisted from at least
medieval times.</p>
</div>
</front>
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<author><name sortKey="Clamer, C" uniqKey="Clamer C">C Clamer</name>
</author>
<author><name sortKey="Humbert, Jb" uniqKey="Humbert J">JB Humbert</name>
</author>
<author><name sortKey="Mitchell, Pd" uniqKey="Mitchell P">PD Mitchell</name>
</author>
</analytic>
</biblStruct>
<biblStruct><analytic><author><name sortKey="Yossepowitch, O" uniqKey="Yossepowitch O">O Yossepowitch</name>
</author>
<author><name sortKey="Gotesman, T" uniqKey="Gotesman T">T Gotesman</name>
</author>
<author><name sortKey="Assous, M" uniqKey="Assous M">M Assous</name>
</author>
<author><name sortKey="Marva, E" uniqKey="Marva E">E Marva</name>
</author>
<author><name sortKey="Zimlichman, R" uniqKey="Zimlichman R">R Zimlichman</name>
</author>
<author><name sortKey="Dan, M" uniqKey="Dan M">M Dan</name>
</author>
</analytic>
</biblStruct>
<biblStruct><analytic><author><name sortKey="Zach, Va" uniqKey="Zach V">VA Zach</name>
</author>
<author><name sortKey="Tsembalyuk, Si" uniqKey="Tsembalyuk S">SI Tsembalyuk</name>
</author>
<author><name sortKey="Siben, An" uniqKey="Siben A">AN Siben</name>
</author>
</analytic>
</biblStruct>
<biblStruct><analytic><author><name sortKey="Zhou, Xn" uniqKey="Zhou X">XN Zhou</name>
</author>
<author><name sortKey="Lv, S" uniqKey="Lv S">S Lv</name>
</author>
<author><name sortKey="Yang, Gj" uniqKey="Yang G">GJ Yang</name>
</author>
<author><name sortKey="Kristensen, Tk" uniqKey="Kristensen T">TK Kristensen</name>
</author>
<author><name sortKey="Bergquist, Nr" uniqKey="Bergquist N">NR Bergquist</name>
</author>
<author><name sortKey="Utzinger, J" uniqKey="Utzinger J">J Utzinger</name>
</author>
<author><name sortKey="Malone, Jb" uniqKey="Malone J">JB Malone</name>
</author>
</analytic>
</biblStruct>
<biblStruct><analytic><author><name sortKey="Zuev, Vf" uniqKey="Zuev V">VF Zuev</name>
</author>
</analytic>
</biblStruct>
</listBibl>
</div1>
</back>
</TEI>
<pmc article-type="research-article"><pmc-dir>properties open_access</pmc-dir>
<front><journal-meta><journal-id journal-id-type="nlm-ta">Mem Inst Oswaldo Cruz</journal-id>
<journal-id journal-id-type="iso-abbrev">Mem. Inst. Oswaldo Cruz</journal-id>
<journal-id journal-id-type="publisher-id">mioc</journal-id>
<journal-title-group><journal-title>Memórias do Instituto Oswaldo Cruz</journal-title>
</journal-title-group>
<issn pub-type="ppub">0074-0276</issn>
<issn pub-type="epub">1678-8060</issn>
<publisher><publisher-name>Instituto Oswaldo Cruz, Ministério da Saúde</publisher-name>
</publisher>
</journal-meta>
<article-meta><article-id pub-id-type="pmid">26602874</article-id>
<article-id pub-id-type="pmc">4708016</article-id>
<article-id pub-id-type="doi">10.1590/0074-02760150156</article-id>
<article-categories><subj-group subj-group-type="heading"><subject>Articles</subject>
</subj-group>
</article-categories>
<title-group><article-title>Opisthorchiasis in infant remains from the medieval Zeleniy Yar burial
ground of XII-XIII centuries AD</article-title>
</title-group>
<contrib-group><contrib contrib-type="author"><name><surname>Slepchenko</surname>
<given-names>Sergey Mikhailovich</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>1</sup>
</xref>
<xref ref-type="corresp" rid="c01"><sup>+</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Gusev</surname>
<given-names>Alexander Vasilevich</given-names>
</name>
<xref ref-type="aff" rid="aff2"><sup>2</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Ivanov</surname>
<given-names>Sergey Nikolaevich</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>1</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Svyatova</surname>
<given-names>Evgenia Olegovna</given-names>
</name>
<xref ref-type="aff" rid="aff3"><sup>3</sup>
</xref>
</contrib>
</contrib-group>
<aff id="aff1"><label>1</label>
Siberian Branch of the Russian Academy of Sciences, Institute for Problems of the Development of the North, Tyumen, Siberia, Russia</aff>
<aff id="aff2"><label>2</label>
YaNAO Arctic Research Center, Archeology Department, Archeology and Ethnology Sector, Salekhard, YaNAO, Russia</aff>
<aff id="aff3"><label>3</label>
Institution of Culture of Sverdlovsk Region, Center for Protection and Use of Monuments of History and Culture of Sverdlovsk Region, Scientific and Production Center, Ekaterinburg, Urais, Russia</aff>
<author-notes><corresp id="c01"><label>+</label>
Corresponding author: <email>s_slepchenko@list.ru</email>
</corresp>
</author-notes>
<pub-date pub-type="epub-ppub"><month>12</month>
<year>2015</year>
</pub-date>
<pmc-comment>Fake ppub date generated by PMC from publisher
pub-date/@pub-type='epub-ppub' </pmc-comment>
<pub-date pub-type="ppub"><month>12</month>
<year>2015</year>
</pub-date>
<volume>110</volume>
<issue>8</issue>
<fpage>974</fpage>
<lpage>980</lpage>
<history><date date-type="received"><day>21</day>
<month>4</month>
<year>2015</year>
</date>
<date date-type="accepted"><day>23</day>
<month>10</month>
<year>2015</year>
</date>
</history>
<permissions><license license-type="open-access" xlink:href="http://creativecommons.org/licenses/by/4.0/"><license-p>This is an Open Access article distributed under the terms of the Creative
Commons Attribution License, which permits unrestricted use, distribution, and
reproduction in any medium, provided the original work is properly
cited.</license-p>
</license>
</permissions>
<abstract><p>We present a paleoparasitological analysis of the medieval Zeleniy Yar burial ground
of the XII-XII centuries AD located in the northern part of Western Siberia. Parasite
eggs, identified as eggs of <italic>Opisthorchis felineus</italic>
, were found in the
samples from the pelvic area of a one year old infant buried at the site. Presence of
these eggs in the soil samples from the infant’s abdomen suggests that he/she was
infected with opisthorchiasis and imply consumption of undercooked fish. Ethnographic
records collected among the population of the northern part of Western Siberia reveal
numerous cases of feeding raw fish to their children. Zeleniy Yar case of
opisthorchiasis suggests that this dietary custom has persisted from at least
medieval times.</p>
</abstract>
<kwd-group><kwd>Opisthorchis felineus</kwd>
<kwd>paleoparasitology</kwd>
<kwd>paleopathology</kwd>
<kwd>Western Siberia</kwd>
<kwd>health status</kwd>
<kwd>food processing</kwd>
</kwd-group>
<counts><fig-count count="3"></fig-count>
<table-count count="0"></table-count>
<equation-count count="0"></equation-count>
<ref-count count="57"></ref-count>
<page-count count="1"></page-count>
</counts>
</article-meta>
</front>
<body><p>Paleoparasitological analysis can be carried out using a wide range of archaeological and
biological objects, including samples from the pelvic/abdominal areas, coprolites, hair,
mummified tissues, and even skeletal remains (<xref rid="B2" ref-type="bibr">Araújo &
Ferreira 1996</xref>
, <xref rid="B9" ref-type="bibr">Bouchet 1997</xref>
,<xref rid="B23" ref-type="bibr">Le Bailly et al. 2005</xref>
, <xref rid="B4" ref-type="bibr">Araújo et al. 2008</xref>
). Identification of endoparasites can complement
archaeological data on the paleodiet, subsistence practices, and food processing
techniques, as well as trace migration patterns and help to reconstruct community health of
prehistoric populations (<xref rid="B34" ref-type="bibr">Reinhard 1988</xref>
, 19,<xref rid="B32" ref-type="bibr">1992a</xref>
, <xref rid="B35" ref-type="bibr">b</xref>
, <xref rid="B2" ref-type="bibr">Araújo & Ferreira 1996</xref>
, 20,<xref rid="B3" ref-type="bibr">2000</xref>
, <xref rid="B17" ref-type="bibr">Horne & Tuck 1996</xref>
,
<xref rid="B10" ref-type="bibr">Bouchet et al. 2001</xref>
,<xref rid="B36" ref-type="bibr">Reinhard & Araújo 2008</xref>
, <xref rid="B19" ref-type="bibr">Jaeger et
al. 2013</xref>
, <xref rid="B44" ref-type="bibr">Slepchenko & Ivanov 2015</xref>
,
<xref rid="B53" ref-type="bibr">Yeh et al. 2015</xref>
).</p>
<p>Paleoparasitological research is still nascent in Russia. Arkadiy Savinetsky and Aleksandr
Khrustalev in 2013 presented a meta-analysis of endoparasites found in the animal faecal
depositions from caves with archaeological deposits dating from as early as 40,000 years
ago to XX century. Their study identified helminth eggs belonging
to<italic>Nematodirus</italic>
sp., <italic>Oxyuris</italic>
(<italic>Oxyurida</italic>
),
<italic>Fasciola</italic>
sp.,<italic>Dicrocoelium</italic>
sp.,
<italic>Trichuris</italic>
, <italic>Capillaria</italic>
sp.,
<italic>Diphyllobothrium</italic>
sp., <italic>Opisthorchis felineus</italic>
,
<italic>Alaria alata</italic>
, and <italic>Dioctophyma renale</italic>
. The diversity of
helminths in the animal faeces provided insights into the subsistence practices of the
early humans and hazards of animal farming in those regions.</p>
<p>Paleoparasitological analysis of dog coprolites from Maray I settlement (dating to 2645 ±
30 BP), located in the forest-steppe zone of West Siberia, revealed larvae
of<italic>Strongyloides papillosus</italic>
, <italic>Strongyloides westeri</italic>
, and
<italic>Strongyloides stercoralis</italic>
(<xref rid="B55" ref-type="bibr">Zach et al.
2011</xref>
, <xref rid="B46" ref-type="bibr">Tsembalyuk 2013</xref>
), suggesting heavy
parasitic loads in the human settlements of the region. Recent analysis of the XVII century
soil and dog coprolites samples from Mangazeya, the earliest Russian town located beyond
the Arctic Circle in West Siberia. The eggs of <italic>O. felineus</italic>
,
<italic>Diphillobathrium latum</italic>
, <italic>Trichocephalus</italic>
sp.,
<italic>Toxocara canis</italic>
, and <italic>Fasciola hepatica</italic>
were identified
there (<xref rid="B49" ref-type="bibr">Vizgalov et al. 2013</xref>
).</p>
<p>The only paleoparasitological investigation of the recent indigenous populations from
Western Siberia was carried out on the samples from the pelvic area from the XVII-XIX
centuries Selkup Kikki-Akki burial site. Tapeworm eggs of
<italic>Diphyllobothrium</italic>
sp., a typical fish endoparasite, showed that uncooked or
undercooked fish served as the primary source of intestinal parasites in Selkup communities
(<xref rid="B44" ref-type="bibr">Slepchenko & Ivanov 2015</xref>
). This finding
corroborated the ethnographic records that the Selkups consumed large quantities of raw or
minimally processed fish (<xref rid="B22" ref-type="bibr">Khomich et al. 2002</xref>
,<xref rid="B47" ref-type="bibr">Tuchkova 2013</xref>
). The absence of <italic>O.
felineus</italic>
, a fish endoparasite common in Ob and Irtysh river basins, in samples
from the Kikki-Akki burial ground suggested that Selkups from Kikki-Akki rarely migrated to
the Ob and Irtysh region for fishing (<xref rid="B54" ref-type="bibr">Yossepowitch et al.
2004</xref>
, <xref rid="B8" ref-type="bibr">Bonina & Fedorov 2010</xref>
, <xref rid="B28" ref-type="bibr">Mordvinov et al. 2012</xref>
). Thus, the Selkups migration
routes were probably limited to the nearby Taz River Basin and, perhaps, the Yenisei and
the Pur river basins which lack<italic>Opisthorchis</italic>
(<xref rid="B44" ref-type="bibr">Slepchenko & Ivanov 2015</xref>
).</p>
<p>Here, we present an analysis of helminth eggs from the soil samples collected from the
pelvic and abdominal area of the child buried in grave 48 (hereafter M48) of the Zeleniy
Yar cemetery dated to between XII-XIII centuries. The Zeleniy Yar archaeological site is
located in the Cisuralian area of Yamalo-Nenets Autonomous Okrug in the north of Western
Siberia (<xref ref-type="fig" rid="f01">Fig. 1</xref>
). It is situated on a flood plain
island between the Poluy River and the Gorny Poluy anabranch. Remains of an early
metallurgy workshop, including two melting furnaces dating to VI-VII centuries AD, have
been recovered from the site. Two associated burial grounds have been dated to the VIII-IX
centuries and the XII-XIII centuries.</p>
<p><fig id="f01" orientation="portrait" position="float"><label>Fig. 1</label>
<caption><title>: location the archaeological site Zeleniy Yar. Distribution of burials on the
archaeological site Zeleniy Yar in 2014. The black point is marked the place of
sampling in the burial 48.</title>
</caption>
<graphic xlink:href="0074-0276-mioc-110-8-0974-gf01"></graphic>
</fig>
</p>
<sec sec-type="materials|methods"><title>MATERIALS AND METHODS</title>
<p>The site was excavated by the authors during the 2014 field season. Four burials dating
from the XII-XIII centuries were excavated and analysed at the same time. Samples were
collected from M48, since it was the only burial that remained intact and undisturbed by
carnivores.</p>
<p>Burial M48 contained remains of an infant with an estimated age around one year, based
on dental eruption and skeletal development. The body was in supine position with the
head placed at a northwest orientation. The infant’s arms were stretched along the body
with the palms positioned on the thighs. The neck was bent, so that the chin was pressed
to the chest, suggesting that there was some support made from perishable material was
placed under the head. The infant was wrapped in a fur garment adorned with copper
plates, which was further wrapped in a hide with fur and a layer of birch bark (<xref rid="B16" ref-type="bibr">Gusev 2015</xref>
).</p>
<p>Since the infant’s sacrum, the os coxae and lumbar vertebra were completely decomposed,
the sample was collected from the abdominal region (<xref ref-type="fig" rid="f02">Fig.
2</xref>
). The sample weighed about 30 g and was vacuum-packed in the field. In
addition, a 50 g control sample was taken from the vicinity of infant’s head at the same
depth as the abdominal sample.</p>
<p><fig id="f02" orientation="portrait" position="float"><label>Fig. 2</label>
<caption><title>: infant skeleton was excavated at Zeleniy Yar and place of sampling. a:
the place of abdomen where the soil sample was collected for the
paleoparasitological study. b: the place where the control soil sample was
collected.</title>
</caption>
<graphic xlink:href="0074-0276-mioc-110-8-0974-gf02"></graphic>
</fig>
</p>
<p>In the laboratory, 3% sodium hydroxide solution was added to the dry sample (<xref rid="B15" ref-type="bibr">Fry 1985</xref>
, <xref rid="B11" ref-type="bibr">Dufour
& Le Bailly 2013</xref>
). In an hour and a half, the liquid was sifted through a
sieve, filled into a plastic test tube, and centrifuged for 7 min (1,500 revolutions per
min); distilled water was added to achieve neutral pH level. Upon completing this
cleaning procedure, we added a rich sodium nitrate solution (1.38-1.40 g/cm<sup>3</sup>
)
to the residue. Sample separation was performed in the same centrifugal tubes. After
multiple centrifuge cycles with 0.5% Na<sub>3</sub>
PO<sub>4</sub>
aqueous solution and
glycerin at a temperature of 22 degrees, we gathered the supernatant fraction. Having
just a few organic particles at hand, we still managed to prepare 20 microslides,
following the recommended standard methods (<xref rid="B33" ref-type="bibr">Reinhard et
al. 1986</xref>
, <xref rid="B5" ref-type="bibr">Araújo et al. 1998</xref>
).
Microscopic examination was conducted using AxioSkop 40 and MicMed 2 var.2. microscopes
under 80X and 400X magnification. Measurements were obtained using AxioVision 4.6 and
Scope Photo 3.0 software.</p>
</sec>
<sec sec-type="results"><title>RESULTS</title>
<p>The microscopic examination of the slides revealed four helminth eggs of an oval shape
and of light yellow colour. The operculums of eggs were absent. Some eggs had slight
shoulders at the area of operculum attachment. At the pole opposite to operculum, there
was a knob. The eggs measured 34.25-32.39 μm in length and 24.5-18.01 μm in width. Based
on their morphology and size, these eggs belong to the trematodes group of <italic>O.
felineus</italic>
(<xref ref-type="fig" rid="f03">Fig. 3</xref>
). The control sample
was free of eggs. Epidemiologic records indicate a high incidence of opisthorchiasis
among the modern-day populations of the area where the Zeleniy Yar burial ground is
located (<xref rid="B18" ref-type="bibr">Istomin et al. 2003</xref>
), corroborating our
interpretation.</p>
<p><fig id="f03" orientation="portrait" position="float"><label>Fig. 3</label>
<caption><title>: eggs suggestive of <italic>Opisthorchis felineus</italic>
found in infant
remains from the medieval Zeleniy Yar burial ground of XII-XIII centuries
AD.</title>
</caption>
<graphic xlink:href="0074-0276-mioc-110-8-0974-gf03"></graphic>
</fig>
</p>
</sec>
<sec sec-type="discussion"><title>DISCUSSION</title>
<p><italic>Differential diagnosis</italic>
- In order to identify species affiliation of
the eggs, we performed a differential diagnosis. The eggs found in the samples from the
burial may belong to several different genera of helminths. Morphological
characteristics such as an oval shape, light yellow colour, size, and knob have to be
further analysed with the aid of differential diagnosis which involves comparing
helminth eggs of the cestodes <italic>Diphyllobothrium</italic>
sp. and of the
trematodes <italic>Clonorchis sinensis</italic>
, <italic>Opisthorchis
viverrini</italic>
, <italic>Metorchis bilis.</italic>
</p>
<p>Diphyllobothriasis is widespread throughout Western Siberia. The Cisuralian area of
Yamalo-Nenets Autonomous Okrug (with Zeleniy Yar burial ground there) has the highest
incidence of this helminth infection among humans in the region. Some records show 340.3
cases per 100,000 people (<xref rid="B38" ref-type="bibr">Rospotrebnadzor State Reports
2011</xref>
). In the Ural Mountain area and Eastern Siberia, <italic>D.
latum</italic>
is the most common fish tape worm infecting humans. In Western Siberia
<italic>Diphyllobothriumdendriticum</italic>
and
<italic>Diphyllobothriumditremum</italic>
are also common in humans, although the
epidemiological impact of the latter on the local human populations is minimal (<xref rid="B52" ref-type="bibr">Yastrebov 2013</xref>
).</p>
<p>Having the same colour, elliptic shape, and knob, <italic>Diphyllobothrium</italic>
sp.
eggs look superficially similar to the eggs of<italic>Opisthorchis</italic>
.
Nevertheless, we excluded the tapeworm eggs as the infection source, because of their
bigger size. Typical<italic>Diphyllobothrium</italic>
eggs measure 58-75 μm x 40-50 μm
(<xref rid="B6" ref-type="bibr">Ash & Orihel 2007</xref>
), considerably larger
than the 24.5-18.01 μm eggs reported here.</p>
<p>Trematodes, <italic>C.sinensis</italic>
and <italic>O.viverrini,</italic>
also produce
eggs that are morphologically very similar to the observed eggs (<xref rid="B20" ref-type="bibr">Kaewkes et al. 1991</xref>
, <xref rid="B56" ref-type="bibr">Zhou et al.
2007</xref>
). Their size falls within the same range as that of the eggs we have
found (29 μm x 17 μm and 27 μm x 15 μm, respectively). Eggs of trematodes are
ovoid-shaped, longish, yellow-brown, and have shoulders at the place of an operculum
attachment and a knob at the opposite egg pole (<xref rid="B39" ref-type="bibr">Sadun
1955</xref>
, <xref rid="B24" ref-type="bibr">Liu & Chen 1998</xref>
). Therefore,
excluding <italic>C. sinensis</italic>
and<italic>O. viverrini</italic>
is difficult.
However, the epidemiologic records show that the trematodes <italic>C. sinensis</italic>
and <italic>O.viverrini</italic>
are unlikely to be the source of infection. Although
both helminths are present in Southeast Asia, Korea, and China (<xref rid="B31" ref-type="bibr">Posokhov 2004</xref>
, <xref rid="B25" ref-type="bibr">Lun et al.
2005</xref>
,<xref rid="B45" ref-type="bibr">Sripa et al. 2007</xref>
), they are
nonexistent in Western Siberia (<xref rid="B31" ref-type="bibr">Posokhov 2004</xref>
).
The only known case of clonorchiasis in Russia has been documented in the Amur River
Basin. Therefore, despite the morphological similarity to the recovered eggs, the
trematodes <italic>C.sinensis</italic>
and <italic>O.viverrini</italic>
are unlikely to
be the source of the infection, albeit these cannot be completely ruled out.</p>
<p>The eggs present in the M48 sample are also morphologically similar to eggs of<italic>M.
bilis</italic>
, a helminth from family Opisthorchidae that is present in Western
Siberia. Since eggs of <italic>O. felineus</italic>
and <italic>M. bilis</italic>
cannot
be differentiated by any common medical and parasitological methods, it is likely that
some of the diagnosed opisthorchiasis infection in Western Siberia is caused by
metorchosis infection or by both (<xref rid="B43" ref-type="bibr">Skrjabin & Petrov
1950</xref>
, <xref rid="B42" ref-type="bibr">Sidorov 1983</xref>
, <xref rid="B37" ref-type="bibr">Romashov et al. 2005</xref>
). However, genus
<italic>Metorchis</italic>
is more commonly present in the southern territory of
Western Siberia, while <italic>O. felineus</italic>
has been recorded in its northern
part (<xref rid="B14" ref-type="bibr">Fattakhov 1996</xref>
). Therefore, final animal
hosts and humans are predominantly infected with opisthorchiasis in the northern part of
Western Siberia, with its highest rate in the Middle Ob Area, whilst metorchosis
infection rate increases towards the southern regions of Siberia (<xref rid="B14" ref-type="bibr">Fattakhov 1996</xref>
). A very low incidence of metorchosis in the lower
course of the Ob River, where Zeleniy Yar burial ground is located, has been documented.
This low occurrence of metorchosis can be explained by a low frequency
of<italic>Bethynia tentaculata</italic>
(family Bithyniidae,
genus<italic>Bethynia</italic>
) molluscs that serve as the principal first
intermediate host for metorchosis. Although <italic>Codiella inflate</italic>
(family
Bithyniidae, genus <italic>Bethynia</italic>
), the secondary intermediate host of
metorchosis, is present in the region, this mollusc has a low susceptibility of
metorchosis, limiting its propagation (<xref rid="B14" ref-type="bibr">Fattakhov
1996</xref>
).</p>
<p>A high frequency of opistarchosis infection is recorded among the modern-day populations
of the Cisuralian area of Yamalo-Nenets Autonomous Okrug. In 2003, the prevalence rate
was 2,585 cases per 100,000 people (<xref rid="B18" ref-type="bibr">Istomin et al.
2003</xref>
). Among children under the age of 14, opistarchosis was present in 110
individuals out of 100,000 (<xref rid="B38" ref-type="bibr">Rospotrebnadzor State
Reports 2011</xref>
). For comparison, the prevalence rate for opistarchosis in the Ob
River tributaries is 10-104 cases per 1,000 people (<xref rid="B21" ref-type="bibr">Karpenko et al. 2008</xref>
). Up to 100% of the indigenous people, among Khanty,
Mansi, and Nenets ethnic communities of the Ob and Irtysh basins in West Siberia are
infected with these helminths (<xref rid="B41" ref-type="bibr">Schustov et al.
2002</xref>
). Such a high incidence of opistarchosis among indigenous people of the
reason is caused by the heavy parasitic loads found in fish of Ob and Irtysh rivers. In
the middle and the lower Ob River Basin, the opistarchosis infection rate in
<italic>Leuciscus idus</italic>
and<italic>Leuciscus icuciscus</italic>
fish is
between 80-100%. The invasion degree is 4.5 and 7.5 larvae per gram of muscles, for
<italic>L. idus</italic>
and<italic>L. Icuciscus</italic>
, respectively [<xref rid="B14" ref-type="bibr">Fattakhov (1996)</xref>
(p. 14)]. Moreover, the high
frequency of opistarchosis among the local people is caused by the consumption of raw,
undercooked, or slightly salted fish (<xref rid="B18" ref-type="bibr">Istomin et al.
2003</xref>
).</p>
<p>Thus, we may infer that the helminth eggs in the samples from the Zeleniy Yar burial
ground most likely belonged to the fish tapeworm genus <italic>O. felineus.</italic>
The
presence of <italic>Opisthorchis</italic>
eggs in the samples from the burial of an
infant under one is noteworthy, as it implies early introduction of solid foods into
infant diet. The infant could be infected with opisthorchiasis only by consuming raw or
minimally processed contaminated fish. The incubation period of opisthorchiasis is
approximately three-four weeks after the initial infection of the final host (<xref rid="B50" ref-type="bibr">Vozianova 2000</xref>
). Consequently, we may infer that the
infant from M48 was given raw fish as a nursing supplement at least one month before
his/her death.</p>
<p>The abundance of fish in the rivers of Western Siberia determined the local subsistence
strategies at least since the terminal Neolithic (<xref rid="B48" ref-type="bibr">Tupakhina 2013</xref>
). Large quantities of fish bones were recovered from the Iron
Age Ust-Poluy archaeological site, located in the lower Ob River Basin, suggesting that
fish was an important and possibly the main food source at the time. Similarly, the
medieval Zeleniy Yar archaeological site is also rich in fish deposits (<xref rid="B1" ref-type="bibr">Aleksashenko et al. 2005</xref>
).</p>
<p>According to ethnographic reports (<xref rid="B7" ref-type="bibr">Bartenev 1896</xref>
,
<xref rid="B12" ref-type="bibr">Dunin-Gorkavich 1910</xref>
), the indigenous people
of the northern part of Western Siberia consumed large quantities of raw fish. In 1715,
the Russian ethnographer Gregory Novitsky recorded that the population of the Ob River
Basin consumed fish, including fish intestines, in large amounts (<xref rid="B57" ref-type="bibr">Zuev 1947</xref>
, <xref rid="B30" ref-type="bibr">Novitsky 1989</xref>
).
People ate considerable quantities of fish liver oil, a local specialty food. Diet
included fresh raw fish in the summer and frozen raw fish in the winter. The same
subsistence practice was described by ethnographer Vasily Zuev in 1771-1772 (<xref rid="B57" ref-type="bibr">Zuev 1947</xref>
). An XVIII-century historian Gerhard
Miller (1742-1746) wrote about the practice of feeding raw fish to young children among
Nents. Nents children over one year old were given deer oil and chopped fish in order to
get them accustomed to eating raw food (<xref rid="B26" ref-type="bibr">Miller
1999</xref>
, <xref rid="B27" ref-type="bibr">2000</xref>
, <xref rid="B13" ref-type="bibr">Ehlert 2006</xref>
). Likewise, the Ostyaks (also known as Khanty) fed adult
food to children. Furthermore, Russian historian Constantine Nosilov recorded
consumption of several fish species, including <italic>Stenodus leucichthys</italic>
,
<italic>L. idus</italic>
, <italic>Rutilus rutilus</italic>
, <italic>Lota
maculosa</italic>
, <italic>Esox lucius</italic>
, <italic>Perca fluviatilis</italic>
,
<italic>Gymnocephalus</italic>
by Khanty (<xref rid="B29" ref-type="bibr">Nosilov
1937</xref>
). Some of these species, such as<italic>L. Idus</italic>
and <italic>R.
rutilus</italic>
, could be carriers of<italic>O. felineus</italic>
larvae (<xref rid="B51" ref-type="bibr">WHO 1995</xref>
), serving as the source of human infection
when consumed raw.</p>
<p>The <italic>Opisthorchis</italic>
eggs presence in the samples from the infant’s burial
in the Zeleniy Yar burial ground reveals a dietary custom of consuming raw or
undercooked fish during the Middle Ages in Western Siberia. Opisthorchiasis infection
observed in the very young infant indicates early supplementation of breast milk with
minimally processed fish. Ethnographic records from the northern part of Western Siberia
corroborate these findings, revealing numerous cases of feeding raw fish to their
children, which suggests that this dietary practice has considerable antiquity.</p>
</sec>
</body>
<back><ack><title>ACKNOWLEDGEMENTS</title>
<p>To DSc Adauto Araujo, PhD Vladimir Adaev, PhD Matthieu Le Bailly, for supporting, and to
PhD Ekaterina Pechenkina and Prof Ron Pinhasi, who improved the quality of our
paper.</p>
</ack>
<fn-group><fn fn-type="financial-disclosure"><p>Financial support: RHCF (13-01-00097 - Ethnodemographic, bioanthropological and
archaeological complex study Taz Nenets and Selkup), RFBR (13-06-00158 А - Features
of physical development of Aboriginal and old residents of Siberia, in the light of
adaptation options)</p>
</fn>
</fn-group>
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