J Vet Res 66, 591-597, 2022

DOI:10.2478/jvetres-2022-0056

Prevalences and characteristics of Trichuris spp. infection

in sheep in pastoral areas of the Tianshan, Xinjiang, China

Lixia Wang1*, Guowu Zhang1*, Yuhang Fu1*, Chengcheng Ning1, Zhiyuan Li1,
Huisheng Wang2, Jinsheng Zhang2, Yunxia Shang1, Yaoqiang Sun1,
Xiaoxing Huang1, Xuepeng Cai3, Xianzhu Xia1, Qingling Meng1, Jun Qiao1
1Collegeof Animal Science and Technology, Shihezi University, Shihezi, Xinjiang 832003, China
2Centerfor Animal Disease Prevention and Control, Tacheng, Xinjiang 834700, China
3State Key Laboratory of Veterinary Etiological Biology, Lanzhou Veterinary Research Institute,

Chinese Academy of Agricultural Sciences, Lanzhou, Gansu 730046, China

[email protected]

Received: April 11, 2022 Accepted: October 11, 2022

Abstract

Introduction: Nematodes of the Trichuris genus are commonly reported parasites that can cause trichuriasis in many animals,
which leads to inflammation, intestinal bleeding and reductions of productivity in livestock. Knowledge of the prevalence
of Trichuris infestation in the Tianshan ovine population and of the nematode species parasitising the population is not exhaustive,
and this study aimed to expand the knowledge. Material and Methods: A total of 1,216 sheep slaughtered in five pasture areas in
the Tianshan Mountains of Xinjiang were investigated and a phylogenetic analysis based on the mitochondrial cox1 gene was
performed to clarify the genetic relationships of the various Trichuris species. Results: Sheep totalling 1,047 were infected with
Trichuris spp. establishing the rate at 86.1%. Using a morphological protocol, six documented and one undefined species were
identified, namely T. gazellae, T. lani, T. ovina, T. longispiculus, T. concolor, T. discolor and Trichuris sp. Among them, T. gazellae
and T. lani were the dominant species, accounting for 34.5% and 31.0% of Trichuris spp., respectively. Phylogenetic analysis
divided the detected species of Trichuris spp. into two genetic clades (clade I and clade II). The six documented species that can
infect sheep and the undefined species were clustered into clade I, with inter- and intra-species genetic diversity apparent.
Conclusion: This survey described in detail the morphological characteristics of six known and one undefined species of Trichuris,
which not only enriched the taxonomic information on record regarding Trichuris spp., but also provided valuable epidemiological
data for the prevention and control of trichuriasis in sheep.

Keywords: sheep, Trichuris spp., prevalence and characteristics, phylogenetic analysis.

Introduction humans and various animals and are rightfully accorded

medical and veterinary importance (9, 11, 14, 18). Since
Nematodes of the Trichuris genus can parasitise the Roederer first named the genus in 1761, so far at least
cecum and colon of humans, cattle, sheep, pigs and other 24 Trichuris species have been documented in ruminants
animals, causing trichuriasis (also known as whipworm (26, 27). In 2012, 415 domesticated adult ruminants
disease), which is harmful to human and livestock health were investigated for evidence of gastrointestinal
and livestock production (2, 15, 23, 28). In ruminants, protozoan and helminthic infections in India and
Trichuris spp. infection can cause chronic cicatricial a 9.15% infection rate of T. trichiura was noted (3).
inflammation of the cecum and colon, resulting in Xinjiang is one of the most important sheep farming
wasting, anaemia and even death (7, 24). Currently, the regions in China, with a current stock of 36 million
disease is widespread and globally distributed, seriously sheep. Digestive tract parasitic infections are very
threatening the sustainability and expansion potential of common in sheep and result in serious economic losses
the farming industry (20). to farmers who graze their flocks in the pasture areas of
The Trichuris genus includes several species such Xinjiang. However, the infection status of the region’s
as T. trichiura, T. suis and T. vulpis, which can infect sheep and the prevalent species of Trichuris in them are

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592 L. Wang et al./J Vet Res/66 (2022) 591-597

still unknown. Therefore, the main objective of this study consisted of 21 μL of water, 1 μL of each FP1 and
was to investigate the prevalences of Trichuris spp. in RP1 primer (0.2 μmol/L), 25 μL of 2× Premix Ex Taq
sheep in the Tianshan pasture areas of Xinjiang and and 2 μL of DNA template. The reaction was carried out
characterise Trichuris spp. using morphological and for 35 cycles of 94°C for 40 s, 56°C for 40 s and 72°C
molecular biological protocols. The investigation’s for 35 s followed by extension at 72°C for l0 min. The
findings are hoped to provide valuable epidemiological PCR products were detected using 1.6 % agarose gel
data for the prevention and control of trichuriasis. electrophoresis, purified using a PCR purification kit
(TaKaRa), and sequenced at the Huada Biological
Company (Shenzhen, China). Each product was
Material and Methods sequenced three times. Sequences that were identical
were used for comparisons. Subsequently, a phylogenetic
Overview of the surveyed areas. The five pastoral tree based on the cox1 gene was constructed using the
areas in the Xinjiang Tianshan Mountains investigated neighbour-joining method using MEGA software
in this survey are Urumqi, Yili, Bole, Tacheng and Altay version 7.0 (12).
(Supplementary Fig. S1). The five pastoral areas are Statistical analysis of data. All data were
located between 44° and 48°N and 83° and 88°E. The statistically analysed using GraphPad Prism 5.0 software
region has a temperate continental climate with (GraphPad Software, La Jolla, CA, USA). Continuous
an annual precipitation of 500 to 600 mm and an average and categorical variables were analysed using one-way
annual temperature of −4 to 9°C. The average analysis of variance and chi-squared tests, respectively.
temperatures in summer range from 20 to 25°C and in Differences were considered significant when P < 0.05
winter range from −15 to −25°C. and highly significant when P < 0.01.
Animals surveyed. During 2019–2021, 1,216 sheep
were investigated, of which approximately 70% were
under one year old and which had all been slaughtered Results
in five pastoral slaughterhouses. All of the sheep had
been reared by grazing. All slaughtered sheep were Of the 1,216 sheep examined, 1,047 were infected
sorted, registered and numbered. After slaughter and by Trichuris spp., which equated to an infection rate
evisceration, the large intestine was collected and of 86.1%. Of the five pasture areas, Altai had the sheep
transported at low temperature to the Xinjiang Key with the highest infection rate (91.4%), while Urumqi
Laboratory of Animal Disease Prevention and Control. had the animals with the lowest (80.7%) (Table 1). The
Methods of investigation. Briefly, the collected infection rates were as high as 99.8% for lambs less than
large intestine was placed in a basin pre-filled with one year old and were accompanied in these youngest
saline, the intestine was dissected and the contents animals by an average infection intensity of 17.8
washed out into the liquid, and then the mucosa was Trichuris spp. (All feces in the large intestine).
examined carefully in a sequential manner. Meanwhile, However, the infection in sheep aged one to four years
the washed-out contents were repeatedly sedimented was less prevalent and weaker, with an 80.7% infection
with saline until the liquid ran clear. The sediment was rate and an average intensity of infection of 9.7. Sheep
then taken and the worms carefully examined. Adult over four years old had a prevalence of 38.7% and
Trichuris nematodes were collected and placed in 75% an average intensity of 6.7 Trichuris spp. The survey
alcohol supplemented with 5% glycerol (18, 29). showed that there were no significant differences
Morphological identification of Trichuris spp. between infection rates in different grazing areas
The morphological identification of Trichuris spp. was (P>0.05), while both infection rates and intensity varied
based on the size of the adult male worm, the ratio of significantly (P<0.05) between lambs less than one year
whip to body, the length of the copulatory spine, and the old and adult sheep over four years old (Table 2).
shape and size of the spiny sheath (6, 11, 20, 22, 26, 27). A total of 16,849 Trichuris spp. (7,548 males and
All individuals of Trichuris spp. were subjected to 9,301 females) from sheep were collected in this survey.
morphometrical identification using an Olympus BX53 Six documented species and one undefined species
microscope (Olympus, Tokyo, Japan). of Trichuris, namely T. gazellae, T. lani, T. ovina,
Molecular and phylogenetic analysis of T. longispiculus, T. concolor, T. discolor and Trichuris sp.
Trichuris spp. Primers were designed based on the (Fig. 1), were morphologically identified based on key
conserved sequence of a mitochondrial marker, the characteristics such as the ratio of whip to body, the
cytochrome c oxidase I (cox1) gene. Their sequences length of the copulatory spine and the shape and size of
were FP: 5′-ACYACATAGTAGGTRTCATG-3′ and male spiny sheaths (Table 3). It was indicated that the
RP: 5′-TGATTTTTTGGTCACCCTGAAGTTTA-3′. undefined species of Trichuris obtained from sheep in
Total genomic DNA was isolated from an individual the pastoral areas of the Tianshan in Xinjiang was
male specimen of different Trichuris species with different in its morphological characteristics from
a DNA extraction kit (TaKaRa, Shiga, Japan) according previously reported Trichuris species. The spicule
to the instructions. Then, a PCR was performed to sheath of Trichuris sp. was covered with small spines
amplify the cox1 gene. The PCR reaction system and shaped such that the beginning of the sheath flared
 L. Wang et al./J Vet Res/66 (2022) 591-597 593

and then gradually became thinner, with no spines at the T. longispiculus, ON190110; T. concolor, ON190108;
end. Trichuris gazellae and T. lani were the dominant T. discolor, ON184014; and Trichuris sp., ON189049,
species, accounting for 34.5% and 31.0% of all ON189053 and ON189054. Phylogenetic analysis
Trichuris, respectively. The other species of Trichuris, revealed that Trichuris spp. divided into two genetic
which were T. ovina, T. longispiculus, T. concolor, clades, namely clade I and clade II. The six known
T. discolor and Trichuris sp., accounted for 15.8%, species and the undefined species investigated in this
6.9%, 5.2%, 3.9% and 2.7%, respectively. study were all classified into clade I. However, these
After amplification (Fig. 2) and sequencing of the species shared a higher genetic relatedness with T. muris
cox1 gene of the six known species, it was found to share and T. pampeana, with the exception of T. ovina, which
99.1–99.8% identities with other Trichuris spp. After the displayed a closer genetic relationship with T. navonae.
same steps, the undefined species’ cox1 gene transpired Moreover, the phylogenetic tree based on cox1 gene
to share only 93.21% identity with other Trichuris spp. also indicated that those Trichuris spp. derived from
The cox1 genes of the investigated species of Trichuris sheep had closer genetic relationships with T. trichiura,
were submitted to GenBank and given these accession while they were genetically far from T. suis and
numbers: T. gazellae, ON190112, ON190105 and ON190107; T. vulpis, which supported the morphological
T. lani, ON190106 and ON213215; T. ovina, ON190109; classification in terms of molecular taxonomy.
Table 1. Survey on the prevalences of Trichuris spp. infection in sheep from the Tianshan Mountains pastoral areas in China
Year
Total
2019 2020 2021
Number Number Number Number Number Number Number Number
Pastoral
of sheep of infected of sheep of infected of sheep of infected of sheep of infected
area
surveyed sheep (%) surveyed sheep (%) surveyed sheep (%) surveyed sheep (%)
Urumqi 86 69 (80.2) 84 66 (78.6) 79 66 (83.5) 249 201 (80.7)
Yili 78 70 (89.7) 85 73 (85.9) 82 70 (85.4) 245 213 (86.9)
Bole 85 74 (87.0) 88 74 (84.1) 75 65 (86.7) 248 213 (85.9)
Tacheng 75 65 (86.7) 78 68 (87.2) 88 74 (84.1) 241 207 (85.9)
Altai 72 66 (91.7) 77 71 (92.2) 84 76 (90.5) 233 213 (91.4)
Total 396 344 (86.9) 412 352 (85.4) 408 351 (86.0) 1,216 1,047（86.1)

Table 2. Infection of Trichuris spp. in sheep at different ages

Sheep age (years) <1 1–4 ≥4

Number of sheep surveyed 862 119 235
Number of infected sheep (%) 860 (99.8) a 96 (80.7) a 91 (38.7) b

Different superscript letters (a, b) in the same row indicate significant difference (P < 0.05)

Table 3. Key characteristics used in the identification of Trichuris spp. in sheep from the Tianshan Mountains pastoral areas in China
Length
Species of Trichuris of Whip Length of
Length of of the spicule
which a male was length/body spicule Morphology of the spicule sheath
body (mm) sheath
examined length (mm)
(mm)
Tubular; the spicule sheath surface densely
T. lani 46.5 ± 10.3 1.8/1 3.2–4.5 0.18–0.2 covered with small spines, the outer shape
resembling a baseball bat
Proximal 3/4 of the sheath densely covered
with small spines; spiny part forming
T. gazellae 52.1 ± 6.6 2.2/1 1.5–2.2 0.2–1.2
an expanded part as it approaches the unarmed
part; distal 1/4 thinner, unarmed
Proximal 1/2 of sheath densely covered with
T. ovina 47.4 ± 8.7 2.5/1 0.8–1.2 0.18–0.32
small spines; distal 1/2 unarmed
Surface densely covered with small spines,
T. discolor 45.2 ± 1.8 1.9/1 1.2–1.5 0.18–0.20
sheath end dilated and spherical
Surface densely covered with small spines,
T. longispiculus 45.6 ± 10.4 2.0/1 1.3–2.5 0.21–0.66
sheath ends flared and enlarged

T. concolor 36.8 ± 7.4 2.2/1 1.1–1.5 0.25–0.3 Rod-shaped, densely covered with small spines

Surface covered with small spines; the

beginning of the sheath flares and then
Trichuris sp. 40.5 ± 5.6 2.0/1 1.1–1.5 0.25–0.3
gradually becomes thinner, with no spines at
the end
594 L. Wang et al./J Vet Res/66 (2022) 591-597

Fig.1. Morphological characteristics of the spine and spicule sheath of male specimens of Trichuris spp. from sheep
from the Tianshan Mountains pastoral areas in China. A – gross morphology of Trichuris spp.; B – T. lani;
C – T. gazellae; D – T. ovina; E – T. discolor; F – T. longispiculus; G – T. concolor; H – Trichuris sp.
 L. Wang et al./J Vet Res/66 (2022) 591-597 595

Fig. 2. Amplification of the mitochondrial cox1 gene of Trichuris spp. M – standard DNA marker DL-2000
(2,000, 1,000, 750, 500, 250 and 100 bp); 1–7 – positive samples detected by RT-PCR; 8 – positive control

Fig. 3. Phylogenetic analysis of different species of the Trichuris genus based on the cox1 gene using MEGA 7.0
software (neighbour-joining method, bootstrap values 1,000)

Discussion human primates and cause trichinosis (5, 25, 28). These
helminths have strong resistance to degrading factors in
Trichuris spp. are soil-transmitted helminths, which the external environment because of the thick shells of
can naturally infect a wide range of hosts including their eggs, thus they can spread widely in domestic
rodents, cats, dogs, pigs, ruminants, humans, and non- animals grazing on pasture (5, 7). Since most sheep in
596 L. Wang et al./J Vet Res/66 (2022) 591-597

Xinjiang are mainly grazed, the sheep are very heavily be developed for the identification of species and
infected with digestive parasites. However, the infection elucidation of the genetic diversity of Trichuris spp.
status of sheep and prevalences of Trichuris spp. in them in the future (14, 29).
are still unknown. In summary, this study revealed for the first time
The prevalences of Trichuris species and their that six documented species and one undefined species
infection intensities in sheep were investigated in the of Trichuris were prevalent in sheep in the Tianshan
northern Xinjiang region. Existing studies have pasture areas of Xinjiang, China. These observations
confirmed that there are approximately 24 species of provided valuable morphological and molecular data for
Trichuris which parasitise ruminants (11, 26, 27). In this the control of trichuriasis in sheep.
epidemiological survey, 6 documented species and
1 undefined species of Trichuris were found in sheep in * These authors contributed equally to this study and
Xinjiang and characterised. It is assumed that this should be considered co-first authors.
breadth of species variety may be related to the
frequency of trade in sheep and the geography. Among Conflict of Interests Statement: The authors declare
the nematodes detected, T. gazellae and T. lani were the that there is no conflict of interests regarding the
dominant species, which accounted for 34.5% and publication of this article.
31.0% of the total number of parasites detected,
respectively. The overall infection rate in sheep in the Financial Disclosure Statement: This work was supported
five grazing areas was 86.1% and the highest infection by the National Key Research and Development
rate of 91.4% was in Altai. The prevalences and Program (No. 2017YFD0501200) and the Public Benefit
infection intensity of Trichuris spp. were significantly Sector Project of China (No. 201303037-5).
higher in lambs than those in adult sheep, which may be
related to the incomplete development of the immune Animal Rights Statement: The authors declare that
system in lambs or the immunity to the parasites of adult the experiments on animals were approved by
individuals. the Research and Ethical Committee of Shihezi University
Accurate identification of Trichuris spp. is essential (No. A2019226).
for epidemiological investigations (15, 21). Generally
speaking, the features of Trichuris spp. in females are Acknowledgements: We thank the field staff who
indistinguishable for various species (17). In the present provided the technical support for this study.
study, distinguishing Trichuris females corresponding to
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