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Adeola et al. BMC Genomics (2024) 25:177
https://doi.org/10.1186/s12864-024-10070-2 BMC Genomics
†Adeniyi C. Adeola, Semiu F. Bello, Abdussamad M. Abdussamad,
Rahamon A. M. Adedokun authors contributed equally to this work.
*Correspondence:
Adeniyi C. Adeola
chadeola@mail.kiz.ac.cn
Full list of author information is available at the end of the article
Abstract
Background Prion diseases, also known as transmissible spongiform encephalopathies (TSEs) remain one of the
deleterious disorders, which have aected several animal species. Polymorphism of the prion protein (PRNP) gene
majorly determines the susceptibility of animals to TSEs. However, only limited studies have examined the variation in
PRNP gene in dierent Nigerian livestock species. Thus, this study aimed to identify the polymorphism of PRNP gene
in Nigerian livestock species (including camel, dog, horse, goat, and sheep). We sequenced the open reading frame
(ORF) of 65 camels, 31 village dogs and 12 horses from Nigeria and compared with PRNP sequences of 886 individuals
retrieved from public databases.
Results All the 994 individuals were assigned into 162 haplotypes. The sheep had the highest number of haplotypes
(n = 54), and the camel had the lowest (n = 7). Phylogenetic tree further conrmed clustering of Nigerian individuals
into their various species. We detected ve non-synonymous SNPs of PRNP comprising of G9A, G10A, C11G, G12C,
and T669C shared by all Nigerian livestock species and were in Hardy-Weinberg Equilibrium (HWE). The amino acid
changes in these ve non-synonymous SNP were all “benign” via Polyphen-2 program. Three SNPs G34C, T699C, and
C738G occurred only in Nigerian dogs while C16G, G502A, G503A, and C681A in Nigerian horse. In addition, C50T was
detected only in goats and sheep.
Conclusion Our study serves as the rst to simultaneously investigate the polymorphism of PRNP gene in Nigerian
livestock species and provides relevant information that could be adopted in programs targeted at breeding for prion
diseases resistance.
Keywords Scrapie, Susceptibility, Prion protein gene, Polymorphism, Livestock, Nigeria
Single nucleotide polymorphisms (SNPs)
in the open reading frame (ORF) of prion
protein gene (PRNP) in Nigerian livestock
species
Adeniyi C.Adeola1,2*†, Semiu F.Bello3†, Abdussamad M.Abdussamad4†, Rahamon A. M.Adedokun5†,
Sunday C.Olaogun5, NasiruAbdullahi6, Akanbi I.Mark7, Anyebe B.Onoja8, Oscar J.Sanke9, Godwin F.Mangbon10,
JebiIbrahim11, Philip M.Dawuda12, Adebowale E.Salako13, SamiaKdidi14 and Mohamed HabibYahyaoui14
Content courtesy of Springer Nature, terms of use apply. Rights reserved.
Page 2 of 8
Adeola et al. BMC Genomics (2024) 25:177
Background
Prion diseases also known as Transmissible spongiform
encephalopathies (TSEs) remain one of the deleterious
disorders [1], which have affected several animal spe-
cies [2, 3]. e unique characterization of Prion diseases
is the accumulation of an “infectious” abnormal prote-
ase-resistant isoform (PrPSc) of cellular prion proteins
(PrPC) encrypted by the prion protein (PRNP) gene [4].
e prion gene family consist of four members namely
prion protein gene (PRNP), the prion-like protein gene
(PRND), the shadow of the prion protein gene (SPRN),
and the prion-related gene (PRNT) [5]. Although only
Shadoo (Sho) protein is enclosed by the SPRN gene, and
its structure is similar to the PrP protein. e PRND is
nearly situated in 20kb downstream of the PRNP gene,
and PRND possess a similar structure with PrP [6]. Prion
protein genes are highly maintained among mammals
[7] and predominantly synthesized in cells of the central
nervous system [8]. Although, it is also expressed in dif-
ferent peripheral tissues [9, 10]. Interestingly, in the cen-
tral nervous system and lymphoid tissues, TSE diseases
encompass a neuronal glycoprotein (i.e. Prion protein)
PrPC (encoded by PRNP gene), which is regenerated into
an abnormal protease-resistant protein [11, 12]. Prion
diseases are grouped as sporadic, familial, and infec-
tious forms and contains two exons with second one car-
rying the whole open reading frame (ORF) in humans
[13]. It was reported that about 85% of prion diseases in
humans are Creutzfeldt–Jakob disease (CJD) while 15%
of the prion diseases include familial CJD, Gerstmann–
Straussler–Scheinker syndrome (GSS), and fatal familial
insomnia (FFI) [14–16]. Another study has reported the
nature of the infectious agents- PrP models of resistant
species including dog, rabbit and horses to prion diseases
[17]. e β2-α2 loop contributes to their protein struc-
tural stabilities while salt bridge contributed to structural
stability of horse prion protein [18].
Prion diseases are the sole human neurodegenerative
disorders with true associates with mammals thereby
enabling rodent suitable models to comprehend the
mechanisms of disease transmission and pathogenesis.
Scrapie is a detrimental neurodegenerative prion mal-
ady and has spread across almost all regions worldwide
[19, 20] leading to spongiform brain pathology, brain
deposition of misfolded among others. Known for over
250 years, scrapie is one of the TSE and encompasses
zoonotic bovine spongiform encephalopathy (BSE) in
cattle and Creutzfeldt–Jakob disease (CJD) in humans,
which are regulated by the prion protein-encoding gene
(PRNP) [21–23]. It has been reported that the resistance
to scrapie is intently regulated by SNPs of the PRNP
gene and controlled by the prion disease agent [7, 24],
and the distribution of SNPs at the ORF of PRNP gene
in various species was presented [25]. In 1986, classical
BSE was first reported in United Kingdom (UK) and
has spread through PrPSc affected meat and bone meal.
However, different surveillance approaches have been
adopted to prevent utilization of contaminated feed and
this has drastically reduced the number of classical BSE
cases [26]. It was reported that the insertion of G allele
at codon 46 of SPRN gene in humans with variant CJD
causes a frameshift of this gene and it displays a signifi-
cant disparity in its distribution between healthy controls
and vCJD patients [27]. Moreover, it was reported that
somatic mutation of humans’ PRNP was predicted to be
one of the factors responsible for prion disease [16]. Also,
scrapie could affect small ruminants including sheep and
goats [28]. In addition, most forms of TSEs affect differ-
ent mammalian species but display high dominance in
ruminants such as scrapie in goats and sheep [29].
Our previous studies revealed that the SNP sites at
codons 139S, 146S, 154H, and 193I were presence in
Nigerian goats [30] which have been reported to be
susceptible to scrapie in goats [28, 31], and also codons
154H and 171Q susceptible to classical scrapie in sheep
[32, 33] detected in Nigerian sheep [34].
Camelus dromedarius are vastly found in the semi-
arid northern part of Nigeria and their estimates is about
289,794 heads [35]. ey are basically reared for meat,
milk, wool, source of transportation, beauty spectacle,
and recreational activities [35]. Nigerian village dogs are
one of the major sources of the transmission of infec-
tious diseases [36], horses from Nigeria are useful for
entertainment, polo games, ceremonies, research, riding
etc. [37]. Nigerian sheep are reared in the drier agro-cli-
matic zones of the country with an estimated population
of 27million [38]. ere are four major breeds of Nige-
rian sheep: Yankasa, Uda, Balami, and West Africa Dwarf
[39]. Nigerian goats are hardy, tolerant to trypanosomi-
asis, and adapt easily to the local ecosystem [40]. ere
are three main indigenous breeds of Nigerian goats: West
African Dwarf (WAD), Sokoto Red and Sahelian [41–43].
erefore, this study was designed to understand the
PRNP gene sequence variation in different Nigerian
livestock species and provide insight into their resis-
tance to prion diseases. Herein, we combined the PRNP
sequences of five Nigerian livestock species (camel, dog,
horse, sheep, and goat) and analyzed the prion genes. In
addition, we retrieved the nucleotide sequences of PRNPs
from other mammalians for the SNP analyses.
Results
Haplotype analysis of the 994 sequences of PRNP gene
A total of 994 PRNP gene sequences were analyzed,
including 108 de novo and 886 downloaded from Gen-
Bank. All the PRNP sequences were assigned into 162
haplotypes (Additional File 1). e sheep had the highest
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Adeola et al. BMC Genomics (2024) 25:177
number of haplotypes (n = 54), and the camel had the
lowest (n = 7).
Phylogenetic tree based on number of haplotypes
Based on the 162 haplotypes, 180 individuals includ-
ing Nigerian species and those retrieved sequences were
selected to construct the phylogenetic tree. Figure 1
showed the phylogenetic tree from the analysis of PRNP
sequences of five Nigerian species together with reported
PRNP sequences of Homo sapiens and Macaca mulatta
as outgroups. e phylogenetic tree further confirmed
clustering of Nigerian individuals into their various
species.
Single nucleotide polymorphism (SNPs) of PRNP gene in
the ve Nigerian species
We detected five non-synonymous SNPs of PRNP namely
G9A, G10A, C11G, G12C, and T669C in all Nigerian
species considered when combined with nucleotide
sequences retrieved from public database (Table1). Fur-
ther, we determined the genotype and allele frequencies
of the five non-synonymous SNPs detected in Nigerian
livestock species and were in Hardy-Weinberg Equilib-
rium (HWE) (Table2). Based G34C, T699C, and C738G
occurred only in PRNP of Nigerian dog while C16G,
G502A, G503A, and C681A were identified in Nigerian
horse only. In addition, C50T was detected in goat and
sheep only. Table 1 shows the non-synonymous SNPs
detected in Nigerian livestock species. All SNPs identi-
fied in Nigerian livestock species are listed in Additional
Table1.
Assessment of the eects of the non-synonymous SNPs
PolyPhen-2 is an online tool used to predict the possible
impact of an amino acid replacement caused by nonsyn-
onymous SNPs on the structure and function of proteins
[44]. Based on the polymorphism results, effects of the
five non-synonymous SNPs common in the five Nige-
rian livestock species considered were assessed via Poly-
Phen-2. It was predicted that the amino acid substitution
in the five non-synonymous SNPs was benign (Table3).
Discussion
e polymorphism of the PRNP gene plays a great role
in the susceptibility of animals to prion protein diseases.
In horses, the stability of prion protein is associated with
disease progression.
Previous studies have identified single nucleotide
mutations at codons 136 (A > V), 154 (R > H), and 171
(R > Q/H) of PRNP gene [45, 46]. Interestingly, the varia-
tion of amino acids at codons 141 and 154 were reported
to be related to various forms of classical scrapie by
altering the configuration of prion protein [47, 48]. In
Fig. 1 Phylogenetic tree of PRNP sequences of Nigerian livestock species and other species
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Adeola et al. BMC Genomics (2024) 25:177
addition, the changes in amino acids A to V and Q to
R at codons 136 and 171, respectively were reported to
increase resistance to scrapie in sheep [20, 45].
e susceptibility of small ruminants (i.e. goat and
sheep) to scrapie are affected by the genetic variation of
the PRNP gene. Goats and sheep share about 99% protein
sequence homology for their prion proteins. Although,
the fragments of their amino acids associated with scra-
pie vulnerability are not similar [5, 21]. PRNP genes are
highly polymorphic in goats [49–52], and the distribu-
tions of genotype and haplotype frequencies at codons
139, 146, and 154 were highly associated with vulnerabil-
ity to scrapie in goats [50, 52].
We combined the PRNP sequences of five Nigerian
livestock species (camel, dog, goat, horse, and sheep) and
retrieved sequences of human, monkey, camel, dog, goat,
sheep, goat, mule deer, Rocky Mountain elk and fallow
deer from available databases. We detected 162 haplo-
types using the 994 sequences (Additional File 3). Based
on the phylogenetic tree when Homo sapiens and Macaca
mulatta are outgroups shows the clustering of Nigerian
individuals into their various species (Fig.2). e sheep
had the highest number of haplotypes (n = 54), and the
camel had the lowest (n = 7). We assumed that the Nige-
rian sheep might be more susceptible to prion related
disease than the other four Nigerian livestock species
(goat, dog, horse, and camel).
Further, based on the SNP analysis, we detected five
non-synonymous SNPs of PRNP namely G9A, G10A,
C11G, G12C, and T669C in all Nigerian species consid-
ered as shown in Table1. e result shows that the five
Nigerian livestock species might be susceptible to prion
related diseases. ese SNP sites are unique to the Nige-
rian livestock species considered in this study. Contrarily,
previous studies on polymorphism of PRNP gene in
Nigerian small ruminants, 29 SNPs (14 non-synonymous
and 23 novel SNPs) and 19 SNPs (14 non-synonymous
SNPs with T718C as a novel SNP) were revealed in Nige-
rian goats and sheep, respectively [30, 34]. Recent stud-
ies have reported low variation in dromedary PRNP gene
in Egypt and Iran [53, 54]. Two non-synonymous SNPs
(G205A and G401A) were identified in PRNP gene in
Algerian dromedary [55] but not detected in the present
study for Nigerian camel. It has been reported that dog
are resistance to prion infection due to change of aspara-
gine at codon 163 [56]. In a previous study, the substitu-
tions of amino acids at canine shadow of prion protein
(Sho) were all neutral except 70_71DelAA that was del-
eterious [57]. Previous study on prion protein gene iden-
tified only one non-synonymous SNP at c.525A (N175K)
in oroughbred horse [58]. Based on PolyPhen-2, it was
predicted that the amino acid substitution in the five
non-synonymous SNPs common to all the Nigerian live-
stock species was benign (tolerant).
Conclusion
is preliminary study aims to examine the single nucle-
otide polymorphism (SNP) in the open frame region
(ORF) of PRNP in Nigerian livestock species. Based on
our results, we detected five non-synonymous SNPs of
Table 1 The variation of non-synonymous single nucleotide
polymorphism (SNPs) of PRNP in the ve Nigerian livestock
species
SNP
location
Changes in Amino acid Species
G9A M3K All species
G10A M3K All species
C11G M3K All species
G12C A4S All species
C16G N5K Horse
C24T C8G goat, sheep
G30T M10I All species
G34C V12L Dog
C50T A16V Goat, sheep
A51G T17M Camel, sheep, and goat
C287G T96S/A Dog, goat, and sheep
A296G S98G 21 goat individuals
G340C M113V 2 sheep individuals
T432C S144N Camel
C480G N160E 3 dog individuals
G501A M167V Horse
G502A M167V Horse
G503A M167V Horse
G505C D168S Dog, camel, goat and sheep
A506G D168S 2 sheep individuals
T508G D168S 8 sheep individuals
C510T Y170D Goat and sheep
C522A N174K 24 sheep individuals
A524G N174K Camel
C534T H178R Dog, goat and sheep
T612C
T612G
V204M/I Horse and camel
Dog
G618A M206I Horse, camel, goat and sheep
G660A E220Q 1 individual dog
G662A E220Q Horse and dog
G663A R221Q Horse, camel, goat and sheep
T669C S223Y All species
G670G S223Y Dog and camel
A678C
A678G
Y226F/S Dog
Camel, goat and sheep
T679C Y226F/S Horse
C681A Y227Q Horse
G693A
G693C
S231A Dog, goat and sheep
Camel
T699C M233A Dog
G700A M233A Dog, camel, goat and sheep
T711C
T711G
S237P Horse, camel, goat and sheep
Dog
C738G F246L Dog
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Adeola et al. BMC Genomics (2024) 25:177
PRNP namely G9A, G10A, C11G, G12C, and T669C in
all Nigerian species. We assumed that Nigerian livestock
species might be susceptible to prion related diseases
based on these codons identified in our current study.
Our preliminary study provides baseline information on
prion gene polymorphism in Nigerian livestock species
and subsequent studies will examine the functional rela-
tionship between clinical signals with prion SNPs from
our genomic studies in connection with genotypes of
prion protein. In addition, future studies will incorporate
large sample size, utilize different coat colors, detect the
prevalence of pion protein disease, and functional analy-
ses in PRNP gene in Nigerian animals.
Materials and methods
Samplings and DNA extraction
We collected about 10ml of blood samples from 65 cam-
els (25 males and 40 females) from four states in Nige-
ria including: Kaduna (n = 19 males; n = 26 females),
Sokoto (n = 5 males ; n = 5 females), Kebbi (n = 1 male; n = 7
females), and Katsina (n = 2 females), 31 village dogs from
Oyo (n = 10 males; n = 8 females) and Taraba (n = 6 males;
n = 7 females) and 12 horses from Oyo (n = 5) and Taraba
(n = 7) states (Fig. 2, Additional File 2). During sample
collection, we avoided individuals from clustered popu-
lations. e whole blood samples were stored at -20 ◦C
prior to DNA extraction. Genomic DNA was extracted
at Kunming Institute of Zoology, Chinese Academy of
Sciences (CAS), using the phenol-chloroform method
[59]. We quantified the genomic DNA using the ermo
Scientific™ NanoDrop 2000 spectrophotometer to evalu-
ate its purity. In addition, to check for molecular quality,
we ran gel electrophoresis of the genomic DNA using
a 2% agarose gel against a 2 Kilobase (kb) DNA ladder
marker. In addition, we retrieved nucleotide sequences of
PRNP of 126 sheep [34] and 132 goats [30] from Nigeria,
human, monkey, camel, dog, sheep, goat and horse indi-
viduals from database (Additional File 2).
Polymerase chain reaction (PCR) and DNA sequencing
We amplified the base pairs of the PRNP gene in the ani-
mals to reveal its variable sites. Primers from each animal
were designed based on the nucleotide sequence of the
PRNP gene retrieved from the NCBI website (Additional
Table2). e 25 µl PCR mixture and sequencing reac-
tions contained 1µl of genomic DNA,10 pmol of each
primer, 2.5mM dNTPs and 5 units of Takara Taq DNA
polymerase in a 10 pmol reaction buffer containing 1.5
mM MgCl2.
e PCR was carried out in a thermocycler (detailed
PCR reactions of each species is presented in Additional
File 3. PCR products were purified for sequencing analy-
sis with a QIAquick Gel Extraction Kit (Qiagen, Valencia,
California, USA). e PCR products were bidirectionally
sequenced using an ABI 3730XL sequencer (Applied Bio-
systems, Foster City, California, USA).
Sequences alignment, haplotype, phylogenetic and
statistical analyses
e sequences were aligned with MEGA (v.11.0.8) [60].
Nucleotide and amino acid alignments were produced
using ClustalW and adjusted manually. We computed
genetic distances using MEGA (v.11.0.8). e number
Table 2 Genotype and allele frequencies of the ve non-synonymous SNPs detected in Nigerian livestock species
Genotype frequency, n (%) Allele frequency, n (%) HWE
GG GA AA G A
G9A 0 (0.00) 0 (0.00) 366 (1.00) 0 (0.00) 732 (100.00) > 0.001
M3K
GG GA AA G A
G10A 0 (0.00) 0 (0.00) 366 (1.00) 0 (0.00) 732 (100.00) > 0.001
M3K
CC CG GG C G
C11G 0 (0.00) 0 (0.00) 366 (1.00) 0 (0.00) 732 (100.00) > 0.001
M3K
GG GC CC G C
G12C 0 (0.00) 0 (0.00) 366 (1.00) 0 (0.00) 732 (100.00) > 0.001
A4K
TT TC CC T C
T669C 0 (0.00) 0 (0.00) 366 (1.00) 0 (0.00) 732 (100.00) > 0.001
S223Y
HWE: Hardy Weinberg Equilibrium
Table 3 Measurement of the eect of amino-acid substitutions
of PRNP nonsynonymous SNPs in the ve Nigerian livestock
species using PolyPhen-2
Position AA1AA2Score Prediction
3 M K 0.000 Benign
4 A S 0.001 Benign
223 S Y 0.006 Benign
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Page 6 of 8
Adeola et al. BMC Genomics (2024) 25:177
of haplotypes in the 994 sequences was analyzed using
DnaSP 6 [61]. Further, we determined the distance matri-
ces under the assumptions of Kimura’s two-parameter
model and were adopted to infer dendrograms by the
neighbor-joining method [62]. e confidence values for
individual branches of the resulting tree were determined
by bootstrap analysis with 1000 replicates [63]. e allelic
and genotypic frequencies of the non-synonymous SNPs
common to the five Nigerian species were tested by chi-
square test (χ2) or Fisher’s exact test using SPSS version
21.0 (IBM Corp., Armonk, NY).
Assessment of the eects of the non-synonymous SNPs
e effects of the three (3) nonsynonymous SNPs of
PRNP gene common to the five Nigerian livestock spe-
cies were evaluated using PolyPhen- 2 (https://genetics.
bwh.harvard.edu/pph2/).
Abbreviations
PRNP Prion protein
TSEs Transmissible spongiform encephalopathies
PrPSc Protease-resistant isoform
PrPC Cellular prion proteins
SPRN Shadow of the prion protein gene
PRNT The prion-related gene
CJD Creutzfeldt–Jakob disease
SNPs Single Nucleotide Polymorphism
WAD West African Dwarf
ORF Open reading frame
Supplementary Information
The online version contains supplementary material available at https://doi.
org/10.1186/s12864-024-10070-2.
Supplementary Material 1
Supplementary Material 2
Supplementary Material 3
Supplementary Material 4
Supplementary Material 5
Acknowledgements
We recognize all who assisted in the success of this study.
Author contributions
A.C.A., S.F.B., A.M.A., and R.A.M.A led the project, designed, and conceived the
study. A.C.A., and S.F.B. performed data analysis, interpreted results, prepared,
and developed the manuscript. A.C.A., and S.F.B carried out experiments. A.E.S.,
Fig. 2 Map of Nigeria showing the sampling locations
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Page 7 of 8
Adeola et al. BMC Genomics (2024) 25:177
A.M.A., N.A., R.A.M.A., A.B.O., A.I.M., O.J.S., S.C.O., G.F.M., J.I., P.M.D., S.K., and M.H.Y.
revised the manuscript. A.C.A., R.A.M.A., A.I.M., O.J.S., S.C.O., G.F.M., J.I., A.M.A.,
N.A., A.E.S., P.M.D., A.B.O., S.K., and M.H.Y. performed sampling. All authors
contributed and approved the nal manuscript.
Funding
This work was supported by the Sino-Africa Joint Research Center, Chinese
Academy of Sciences (SAJC202103), and the Animal Branch of the Germplasm
Bank of Wild Species, Chinese Academy of Sciences (the Large Research
Infrastructure Funding). In addition, this work has been successful through
the Chinese Academy of Sciences President’s International Fellowship
Initiative (CAS-PIFI) who provided grant support to Adeola Charles Adeniyi
(2021FYB0006).
Data availability
The nucleotide sequences are available on NCBI with accession numbers:
MZ463488 - MZ463499 for horse, MZ463325 - MZ463355 for dog, and
OK041226 - OK041290 for camel.
Declarations
Ethics approval and consent to participate
All experimental procedures in this present study were performed in
accordance with Research Guidelines for the Institutional Review Board of
Kunming Institute of Zoology, Chinese Academy of Sciences (SMKX-20160524-
119) and current study is approved by the Institutional Review Board of
Kunming Institute of Zoology, Chinese Academy of Sciences (SMKX-20160524-
119). We have complied with ARRIVE at submission.
Consent for publication
Not Applicable.
Competing interests
The authors declare no competing interests.
Author details
1State Key Laboratory of Genetic Resources and Evolution & Yunnan
Laboratory of Molecular Biology of Domestic Animals, Kunming Institute
of Zoology, Chinese Academy of Sciences, Kunming, China
2Sino-Africa Joint Research Center, Chinese Academy of Sciences,
Kunming, China
3Department of Animal Genetics, Breeding and Reproduction, College of
Animal Science, South China Agricultural University, 510642 Guangzhou,
China
4Department of Veterinary Physiology and Biochemistry, Faculty of
Veterinary Medicine, Bayero University, Kano, Nigeria
5Department of Veterinary Medicine, Faculty of Veterinary Medicine,
University of Ibadan, Ibadan, Nigeria
6Department of Biochemistry, Faculty of Basic Medical Sciences, College
of Health Sciences, Bayero University, Kano, Nigeria
7Ministry of Agriculture and Rural Development, Secretariat, Ibadan,
Nigeria
8Department of Virology, College of Medicine, University of Ibadan,
Ibadan, Nigeria
9Taraba State Ministry of Agriculture and Natural Resources, Jalingo,
Nigeria
10Division of Veterinary Oce, Serti, Nigeria
11Department of Veterinary Surgery and Theriogenology, College of
Veterinary Medicine, University of Agriculture Makurdi, Makurdi, Nigeria
12Department of Animal Science, Faculty of Agriculture, National
University of Lesotho, Maseru, South Africa
13Department of Animal Science, Faculty of Agriculture, University of
Ibadan, Ibadan, Nigeria
14Livestock and Wildlife Laboratory, Institut des Régions Arides, Université
de Gabes, Route El Djorf, Km 22.5, 4119 Medenine, Tunisia
Received: 12 June 2023 / Accepted: 31 January 2024
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