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ORIGINAL ARTICLE
Seroprevalence of peste des petits ruminants among unvaccinated small
ruminants in Sokoto State, northwestern Nigeria
M. B. Bello
1
&H. M. Kazeem
2
&S. B. Oladele
2
&M. Y. Fatihu
2
&F. M. Tambuwal
1
&A. H. Jibril
1
Received: 8 March 2018 / Accepted: 21 March 2018
#Springer-Verlag London Ltd., part of Springer Nature 2018
Abstract
In order to determine the current status of peste des petits ruminants (PPR) in Sokoto State, Nigeria, a competitive ELISA kit was
used to detect the presence of antibodies to PPR virus among the unvaccinated sheep and goats from some randomly selected
local government areas (LGAs) in the study area. An overall seroprevalence rate of 45.50% (197/433) was recorded for the
disease in this study. Based on the LGAs sampled, the seroprevalence rates in decreasing order were 68.75% (Sokoto South),
59.10% (Tambuwal), 56.72% (Goronyo), 53.24% (Kware), 33.24% (Bodinga) and 18.60% (Wurno). Our results further revealed
that sheep had a significantly (p< 0.05) higher percentage of the seroprevalence rate (52.41%) than the goats (40.24%) sampled
in this study. Similarly, age group was found to be significantly associated with the seroprevalence rate which was highest among
animals aged 1–2 years (52.49%) followed by those aged less than 1 year old (44.86%) and those aged above 2 years (31.97%).
Lastly, breeds of goats, but not those of sheep considered in this study, were found to be significantly associated with the
seroprevalence rate (p< 0.05). Altogether, our results signify the active circulation of PPR virus in all the geopolitical zones of
the state, and that age, sex, species and location of sampling may constitute the risk factors for the occurrence of the disease in the
study area. Therefore, vaccination using PPR homologous vaccine should be intensified in the study area. Genetic characterisa-
tion of the circulating peste des petits ruminants virus in the study area should also be performed.
Keywords Peste des petits ruminants .ELISA .Seroprevalence .Sokoto .Small ruminants
Introduction
Peste des petits ruminants (PPR) is an acute highly contagious
transboundary viral disease of sheep and goats characterised by
conjunctivitis, occulo-nasal discharge due to respiratory distress,
pyrexia due to viraemia and diarrhoea due to gastroenteritis
(Couacy-Hymann et al. 2007;ElHarraketal.2012). The dis-
ease is regarded as the most important militating factor against
small ruminants’productivity particularly in Asia and Africa,
where more than one billion sheep and goats are said to be at
riskofthedisease(EMPRES2009). In the last two decades, the
host range of the disease expanded beyond its natural hosts
to include several other domestic and wildlife species of animals
(Kumar et al. 2014). For instance, serological evidence of
PPR in cattle and buffalos has been widely reported in
different regions, although typical clinical disease could
not be observed even under experimental conditions
(Haroun et al. 2002; Lembo et al. 2013). However, unlike
in cattle, the disease may have devastating clinical conse-
quences in the camels and many wild small ruminants
where severe illness and high mortality are often observed
(Furley et al. 1987;Hoffmannetal.2012; Kinne et al.
2010).Theroleofthiswidehostrangeintheoverall
epidemiology of the disease is still being investigated.
The aetiology of PPR is a highly pleomorphic enveloped
RNA virus in the genus Morbillivirus and family
Paramyxoviridae. Antigenically, peste des petits ruminants
virus (PPRV) is related to rinderpest, canine distemper, mea-
sles and the dolphin distemper viruses. As a matter of fact, so
close is the rinderpest virus to PPRV that tissue culture rinder-
pest vaccine (TCRV) was extensively used in the early control
of PPR and was only stopped because of the global rinderpest
eradication programme (Roeder et al. 2004). Furthermore,
*M. B. Bello
bbtambuwal@gmail.com
1
Faculty of Veterinary Medicine, Usmanu Danfodiyo University
Sokoto, Sokoto, Nigeria
2
Faculty of Veterinary Medicine, Ahmadu Bello University Zaria,
Zaria, Nigeria
Comparative Clinical Pathology
https://doi.org/10.1007/s00580-018-2711-8
similar to all paramyxoviruses, the genome of PPRV encodes
six structural proteins: nucleoprotein (N), phosphoprotein (P),
matrix protein (M), fusion protein (F), hemagglutinin protein
(H) and large protein (L), and two accessory proteins which
are the V and C proteins (Bailey et al. 2005). To date, four
lineages have been identified based on the partial sequence of
F and N genes and have epidemiologically been associated
with geographic distribution of PPRV. Interestingly, out of
the four lineages, lineage IV shows more evolutionary adap-
tation to small ruminants because of its emergence in novel
hosts and geographic locations (Munir 2014). Virtually, all the
newly reported cases of PPR in new hosts or recently affected
countries are due to lineage IV.
So far, the global distribution of PPR is restricted to Asia
and Africa although the recent description of the disease in
Turkey and other countries on the fringes of the two continents
is seriously threatening the European sheep and goat popula-
tion (Munir 2014; Ozkul et al. 2002). In the continent of
Africa, PPR has been reported in all the sub-regions with the
West Africa having the highest number of reported outbreaks
across the entire continent (Banyard et al. 2010). Indeed, his-
torically, the first description of PPR was in Ivory Coast in
1942 and the virus remained within the West African sub-
region for over three decades before it subsequently emerged
in Oman (Taylor et al. 1990). In Nigeria, PPR has been report-
ed as far back as 1976 by Hamdy and Dardiri (1976)andto
date, the disease remains endemic in the country causing huge
economic losses in the small ruminant industry. Recently, the
occurrence of PPR has been described in different parts of the
country by Luka et al. (2011) and El-Yuguda et al. (2013).
However, the status of the disease in the core northwestern
part of Nigeria is largely unknown. Therefore, this study was
undertaken to determine the current serological status of PPR
among the unvaccinated sheep and goats in different parts of
Sokoto State, which shares an international border with Niger
republic, another PPR endemic country.
Materials and methods
Study area
Sokoto State is located between latitude 12 14° N and longi-
tude 4–6° E in the Sudan savanna zone of Nigeria (Fig. 1). It
forms boundaries with the Republic of Niger to the north,
Kebbi State to the west and southwest and Zamfara State to
the east (NPC 2006). It is divided into three geopolitical zones:
southern zone, central zone and the eastern zone. The state
covers a total land area of about 32,000 km
2
with an estimated
human population of 3,696,999 million (NPC 2006). Because
of the vegetation characterised by sparse fertile land in the state,
majority of the populace are farmers and are involved in either
large-scale livestock farming in the form of institutional farms
or small-scale backyard farming. Annual rainfall is about
550 mm and usually sets in from June to September. The har-
mattan period starts from October to February and the hot
season comes from March to the end of May.
Study design, sample collection and storage
In this cross-sectional study, a multi stage sampling strategy
was adopted. The stages of sampling are zone-local govern-
ment area (LGA) village-house hold-flock of sheep and goats.
All the three zones were involved in the study, and accordingly,
two LGAs were randomly selected from each zone for sera
sampling. Goronyo and Wurno LGAs were chosen in the east-
ern zone while in the central zone, Sokoto South and Kware
were selected by simple random sampling. In the western zone,
the LGAs selected were Tambuwal and Bodinga. From each of
the selected LGA, villages and flocks were conveniently select-
ed based on vehicle accessibility and the consent of the flock
owner. Since no serological test can differentiate vaccinated
from infected sheep and goats, we adopted certain inclusion
criteria, such that samples were only collected from animals
that had no history of previous vaccination. Also, animals less
than 6 months old were not included in the study. Five 5 mL of
blood sample was collected from the jugular veins of sheep and
goats using sterile syringes with 21 gauge hypodermic needles.
The samples were then centrifuged in order to obtain sera which
were stored at −20 °C until examined. A total of 433 samples
were collected from the small ruminants (187 sheep and 246
goats) in all the sampling units in the study area.
Antibody detection
The sera were examined for the presence of anti-PPRV anti-
bodies using a monoclonal antibody-based competitive
enzyme-linked immunosorbent assay (c-ELISA). The princi-
ple of the test is based on the inhibition of binding of the
mouse monoclonal antibodies (Mab), directed against the
hemagglutinin antigen of the PPR virus, in the presence of a
positive serum. The presence of antibodies to PPR virus in the
test serum blocks the reactivity of the monoclonal antibody
resulting in a reduction in the colour following the addition of
enzyme-labelled anti-mouse antibody and substrate.
Test procedure
All reagents used in the test were prepared according to the
manufacturer’s instruction. The antigen (H-PPRV) was first di-
luted in a coating buffer and 50 μL of the diluted antigen was
added to each well of the microtitre plate. The microplates were
then covered and placed in an orbital plate shaker at 37 °C for 1 h
after which they were washed three times with a washing buffer
and blot dry. Forty microlitres of the blocking buffer was added
to all wells of the plate and 10 μL volumes of the test and control
Comp Clin Pathol
sera were added to the appropriate wells. The monoclonal control
wells received 10 μL of the blocking buffer while 60 μLofthe
blocking buffer was added to the conjugate control wells. All
wells, except the conjugate control wells, received 50 μLofthe
Mab. The microplates were again covered and placed on an
orbital shaker at 37 °C for 1 h after which they were washed
three times and blot dry. All wells then received 50 μLofanti-
mouse conjugate and the sides of the plate were tapped to ensure
that the conjugate-working dilution was evenly distributed over
the bottom of each well. The microplates were again covered and
incubated for 1 h at 37 °C with continuous shaking. After three
washings, 50 μL of the chromogen/substrate mixture was added
to all wells, and after 10 min incubation at room temperature,
colour development was stopped by adding 50 μL of stop solu-
tion to all wells. Optical density of the values was read at 492 nm
usinganELISAreader.
The inhibition of binding of the monoclonal antibody in the
presence of the test serum was expressed as percentage inhibi-
tion (PI) estimated from mean optical density using the formula.
PI ¼100‐Optical density of the test wellsðÞ
Optical density of the Mab control wells 100%
Test sera demonstrating mean percentage inhibition values of
50% or greater were considered positive to PPR virus antibodies.
Any value less than this threshold was considered negative.
Statistical analysis
The data obtained from this study were presented in percent-
ages, tables and charts using Microsoft excel 2010. Chi-square
test of independence and odds ratio (OR) were used to deter-
mine the association of the variables (age, sex, species and
breed) with the seroprevalence rates. The value of p<0.05
was considered significant in this study. Inferential statistical
analysis was performed using Graphpad instat software.
Results and discussion
Serological diagnosis is important in the detection of previous
and recent infections of PPR. Therefore, highly sensitive, spe-
cific and reliable diagnostic techniques such as c-ELISA are
desirable to rapidly detect evidences of PPRV infection so that
effective preventive and control measures can be properly
instituted. The present study established the overall PPR sero-
prevalence of 45.5% (197/433) among the unvaccinated small
ruminants found in Sokoto State using c-ELISA. This appears
to be the true serological status of the disease in the study area
since the sampled animals neither have maternal antibodies
nor do they have any history of previous vaccination against
PPR. The study therefore provides current baseline informa-
tion for PPR in small ruminants found in the study area. This
finding implies that a significant number of sheep and goats in
Sokoto State have been exposed to PPR virus suggesting the
active circulation of the virus in different regions in the study
area. Interestingly, antibodies to PPRV were detected in small
ruminants from all the LGAs sampled in this study, suggesting
the presence of the virus in all the geopolitical zones of the
state. The highest prevalence was observed in Sokoto South
LGA (68.75%) while the least seroprevalence rate of 18.60%
Fig. 1 Map of Sokoto State
showing the study area
Comp Clin Pathol
was obtained in Wurno LGA (Table 1) and there is a signifi-
cant statistical association between the seroprevalence rate
and the sampled LGAs (p< 0.05). Furthermore, apart from
being one of the major livestock-producing states in Nigeria,
the study area shares a common international boundary with
Niger republic which is another PPR endemic country
(Kaukarbayevich 2009). Cross border nomadic movement of
small ruminants from Niger republic into the study area cer-
tainly plays an important role in facilitating the transmission
of the virus in the state. This among several other factors could
probably explain the high overall seroprevalence rate of PPR
recorded in the study area.
On the basis of the species, sheep (98/187) were ob-
served to have significantly greater prevalence of anti-
PPRV antibodies (52.41%) than the goats (99/246) whose
seroprevalence rate was 40.24% (p< 0.05). Similar results
were obtained in the semi-arid region of northeastern
Nigeria by Taylor and Abegunde (1979) and El-Yuguda
et al. (2013). This higher seroprevalence of PPR in sheep
recorded in this study does not translate to the disease
being more severe in sheep than in goats. Rather, it could
be attributed to the higher rate of survival in sheep than in
goats following infection with wild-type PPR virus.
Indeed, Truong et al. (2014)andNandaetal.(1996)ob-
served a significantly higher clinical severity due to PPR in
goats compared to sheep. Because most of the goats infect-
ed with PPRV hardly survive the disease, seropositive
goats are less commonly encountered during sampling
compared to sheep with detectable antibodies as a result
of recovery from previous infection. This may explain the
significantly higher seroprevalence rate of PPR observed
in sheep than in the goats in the present study.
As previously observed by Bello et al. (2016), age preva-
lence of anti-PPRV antibodies recorded in this study revealed
a significant association between the seroprevalence rate and
the three age groups considered in this study (p< 0.05). Small
ruminants aged between 1 and 2 years had the highest sero-
prevalence rate (52.49%) followed by those aged less than
1 year (48.46%) while the least seroprevalence rate was ob-
tained in those animals aged above 2 years old. This particular
finding contradicts the finding of Abubakar et al. (2009)who
reported that seroprevalence rate increases with age. It is gen-
erally known that dams infected with PPR virus can passively
transfer maternal antibodies to their young ones (Parida et al.
2015). Although the maternal antibodies progressively decay,
they remain above the protective threshold for up to 3–
4 months (Bodjo et al. 2006) after which susceptibility to
PPR increases with age. This increased PPR vulnerability with
age sequel to the decay of maternal antibodies, may explain
the increase seroprevalence of PPR with age from 0 to 2 years
Table 1 Distribution of PPRV
antibodies among small
ruminants in Sokoto State
according to LGA, species, sex
and age group
Epidemiologic
variable
Number
sampled
Number
positive
Seroprevalence
rate (%)
Odds
ratio
Confidence
interval
pvalue
Location (LGA)
Sokoto South 48 33 68.75 < 0.01
Tambuwal 66 39 59.10
Bodinga 89 30 33.71
Wurn o 86 16 18.60
Kware 77 41 53.24
Goronyo 67 38 56.72
Tot al 43 3 1 97 4 5. 50
Species
Sheep 187 98 52.41 1.64* 1.11–2.40 0.015
Goats 246 99 40.24 1.00
ref
Tot al 43 3 1 97 4 5. 50
Sex
Male 174 68 39.08 1.00
ref
1.05–2.29 0.0358
Female 259 129 49.80 1.55*
Tot al 43 3 1 97 4 5. 50
Age group (years)
< 1 130 63 44.86 0.015
1–2 181 95 52.49
Above 2 122 39 31.97
Overall 433 197 45.50
*means significantly differed from the reference
ref reference
Comp Clin Pathol
in sheep and goats observed in this study. However, further
research is needed to experimentally demonstrate the pattern
of anti-PPRV antibody decline in animals beyond the age of
2years.
Analysis of the data obtained in this study indicates
that female animals had a significantly greater seroprev-
alence rate than their male counterparts (p< 0.05).
Indeed, odds ratio analysis revealed that they are also
more like to develop PPRV antibodies than the male an-
imals (OD = 1.55). This observation is consistent with
the findings by Kihu et al. (2015) who reported a signif-
icantly higher seroprevalence rate of anti-PPRV antibod-
ies in females than in male sheep and goats. Similar
observation was also made by other researchers in differ-
ent countries (Munir 2014; Munir 2015). It is generally
known that male animals are not usually kept in a flock
for a long period of time (Al-Majali et al. 2008). They
are either sacrificed during the annual religious festivities
or even sold out for meat at approximately 1–2 years of
age. In contrast, the female animals may remain in the
flock for breeding purposes over a long period of time.
Therefore, females tend to have greater exposure time
than males in the flock. This may explain the higher
seroprevalence rate obtained among the females in this
study.
Results for the distribution of anti-PPRVantibodies among
the different breeds of goats indicate that the Red Sokoto goats
(47.52%) appeared to have significantly greater prevalence of
PPR virus antibodies than other breeds (Sahelian and Mixed)
sampled in this study (p< 0.05) (Table 2). Genetic factors such
as breed predisposition are believed to be the major factors
that cause the variation in the seroprevalence rates among
different breeds observed in this study. It is possible that Red
Sokoto goats are genetically more susceptible to PPR infec-
tion than the other breeds sampled in the study. In the case of
sheep, there was no statistical association between the sero-
prevalence rate and the breeds considered. A comprehensive
animal trial should be performed to further elucidate the sus-
ceptibility of different breeds of sheep and goats to virulent
PPR purposes in the study area.
Conclusion
The detection of anti-PPRVantibodies among the unvaccinat-
ed small ruminants in all the LGAs sampled in this study is a
clear indication of the active circulation of the virus in north-
western Nigeria. Epidemiologic variables such as age, sex,
species and breeds may serve as risk factors that determine
the outcome ofthe disease inthe study area. Therefore,control
efforts for PPR particularly vaccination with PPR homologous
vaccine should be intensified in the study area. Furthermore,
there is a need to conduct a detailed molecular epidemiologi-
cal study in order to characterise the actively circulating line-
ages in the study area.
Acknowledgements Special appreciation goes to the staff of the Virus
Research Division, National Veterinary Research Institute, Vom, Nigeria,
for their technical assistance in the conduct of this research.
Compliance with ethical standards
Conflict of interest The authors declare that they have no conflict of
interest.
Ethical statements This research does not contain any studies on human
participants. All procedures on animals in this research were carried out
according to the recommendations of the Animal Welfare Committee of
the Faculty of Veterinary Medicine, Ahmadu Bello University, Zaria.
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