Transboundary and Emerging Diseases
ORIGINAL ARTICLE
First Evidence of Peste des Petits Ruminants (PPR) Virus
Circulation in Algeria (Sahrawi Territories): Outbreak
Investigation and Virus Lineage Identification
M. De Nardi1, S. M. Lamin Saleh2, C. Batten3, C. Oura3, A. Di Nardo3 and D. Rossi4
1
2
3
4
Istituto Zooprofilattico Sperimentale delle Venezie, Legnaro (PD), Italy
Sahrawi Veterinary Services, Ministry of Public Health, Sahrawi Arab Democratic Republic, Rabouni, Algeria
Institute for Animal Health, Pirbright, UK
Faculty of Veterinary Medicine, University of Bologna, Bologna, Italy
Keywords:
peste des petits ruminants; outbreak
investigation; lineage IV; Algeria; Sahrawi;
contingency plan
Correspondence:M.
De Nardi. Istituto Zooprofilattico Sperimentale
delle Venezie, Viale dell’Università’ 10, 32050
Legnaro (PD), Italy.
Tel.: +39 347 1376774;
Fax: +39 049 8084360;
E-mail: mdenardi@izsvenezie.it
Summary
Following reports of increased mortality in the small ruminant population of
the Sahrawi territories, western Algeria, between January and May 2010, local
veterinary authorities suspected an outbreak of peste des petits ruminants
(PPR). An investigation was implemented in May 2010 and followed up in
October 2010 in the Sahrawi refugee camps, Tindouf province, with the objective of confirming the circulation of the peste des petits ruminants virus
(PPRV). Laboratory results confirmed the presence of PPRV in 33.3% of the
samples. Sequence analysis revealed that the virus belonged to Lineage IV and
phylogenetic analysis indicated a close relationship (99.3%) with the PPRV isolated during the Moroccan outbreak in 2008.
Received for publication April 30, 2011
doi:10.1111/j.1865-1682.2011.01260.x
Introduction
Peste des petits ruminants (PPR) is one of the most economically relevant diseases of small ruminants in the
regions where it occurs (Rossiter, 2004a; Diallo et al.,
2007) and economic losses can be aggravated by the control measures imposed, which often involve livestock
movement and animal by-products trade restrictions.
Peste des petits ruminants is widespread in Africa, Arabia, the Middle East and in some geographical areas of
Asia, including much of the Indian subcontinent (CFSPH,
2008). Since 2007, more than one billion small ruminants
in Africa and Asia have been considered at risk of being
infected with the peste des petits ruminants virus (PPRV)
(FAO, 2009). The disease is mostly present in developing
countries which often rely heavily on subsistence farming
of small ruminants for trade and food supply. As a consequence, the economic impact of PPR, especially in a naı̈ve
population with mortality rates as high as 50–80%, can
be devastating (Anderson, 1995; Rossiter, 2004a; Diallo
ª 2011 Blackwell Verlag GmbH • Transboundary and Emerging Diseases.
et al., 2007; Banyard et al., 2010). In countries where
PPR outbreaks occur, annual economic losses are in the
range of millions of USD (Kaukarbayevich, 2009; Banyard
et al., 2010).
Peste des petits ruminants is caused by a highly contagious RNA virus (family Paramyxoviridae, genus Morbillivirus) affecting small ruminants such as sheep, goats and
taxonomically related species (CFSPH, 2008). Peste des
petits ruminants virus is genetically similar to other members of the Morbillivirus genus such as measles virus, rinderpest (RP) virus, canine distemper virus and other
viruses affecting aquatic mammals (Banyard et al., 2010).
Historically, PPR and RP have often been confused
because of their similar clinical, pathological and immunological signs (Kaukarbayevich, 2009), even though RP
is a disease of large ruminants and other artiodactyls
(Rossiter, 2004b). Four genetically distinct lineages
(namely, I to IV) of PPRV have been recognized, and
molecular studies have shown that an inherited differentiation exists between non-African and African isolates
1
Peste des Petits Ruminants, Algeria
(Rossiter, 2004a; Banyard et al., 2010). It is still unclear
whether differences between lineages are merely reflecting
geographical speciation or if they are also correlated to
pathogenicity variability between isolates (Banyard et al.,
2010). The virus is transmitted through direct contact
between infected and susceptible populations: the presence of mixed populations (i.e. flock of sheep and goats)
and the introduction of new animals into a flock/herd are
major risk factors for the PPR spread (CFSPH, 2008). In
pastoral areas, livestock trade, nomadic herding (FAO,
2009) and the congregation of susceptible populations
close to watering points during dry seasons and/or in
livestock markets play an important role in spreading the
disease.
The disease is widespread in western, central, eastern and
northern Africa (Banyard et al., 2010; OIE, 2011a), and the
four genetic lineages are all present in different regions of
the continent. In northern Africa, only Libya has not
reported the disease to date (Banyard et al., 2010; OIE,
2011b). In 2008, an extensive epidemic of the PPRV lineage
IV occurred in Morocco. This finding was particularly relevant as it marked further geographical spread of this lineage
outside eastern and western Africa and its first detection in
northern Africa. Furthermore, because of these outbreaks
in Morocco and the existing commercial trade between
Morocco and both Algeria and Spain, the situation raised
huge concern owing to the increased risk of introduction of
the disease into free zones in northern Africa and into Europe (FAO, 2009; Khalafalla et al., 2010).
In March 2011, the Director of the Algerian Veterinary
Services officially notified the World Organization for
Animal Health (OIE) about serologically confirmed cases
of PPR in five Algerian provinces, even though samples
tested negative by reverse transcription – polymerase
chain reaction (RT-PCR) and no clinical signs were
observed. The source of the outbreak was declared
unknown (OIE, 2011b). This was the first official notification of PPR by the Algerian authorities to the OIE,
although serological reactors had previously been detected
in western Algeria in 2005 and 2008 (A. Broglia, unpublished observation; Di Nardo A, Rossi D, Lamin Saleh
S.M, Lejlifa S.M, Hamdi S.J, Sabatini M, Teodori L,
Savini G, Thrusfield M.V, unpublished observation).
In the Tindouf province (western Algeria), a geographical area inhabited by the Sahrawi community, the
local veterinary authorities (Sahrawi Veterinary Services)
were alerted between January and May 2010 by a significant increase in livestock deaths (MoPH, 2010).
Members of the Sahrawi community live in six refugee
camps, named El Aaiun, Awserd, Smara, Dakhla, 27
Febrero and Rabouni, and, with the exception of
Dakhla, they were all severely affected. Furthermore,
signs of severe respiratory disorders associated with
2
M. De Nardi et al.
enteritis, fever and depression in sheep and goats were
reported in all refugee camps, again with the exception
of Dakhla. Young animals seemed to be more affected
(S.M. Lamin Saleh, personal communication). Despite
the clinical picture suggesting a presumptive diagnosis
of pasteurellosis, a disease frequently reported in the
livestock population in the camps because of the rearing condition, the suspicion of an underlying viral disease was strengthened by the high and unusual
mortality rate. Peste des petits ruminants virus was suspected as a possible pathogen causing the reported
increased mortality. The suspicion was supported by the
fact that: a) outbreaks of PPR occurred in 2008 in
Morocco in the areas close to the border with northwestern Algeria; b) PPR antibodies were detected in
small ruminants in 2005 and 2008 in the camps (A. Di
Nardo et al., unpublished observation; A. Broglia,
unpublished observation); c) small ruminants reared in
the camps are normally purchased in Mauritania and
Mali, where the disease is endemic (FAO, 2008); d)
local breeds are considered to be more resistant to PPR
and have been associated with sub-clinical or mild
forms of the disease, which are insufficiently severe to
attract veterinary attention (Rossiter, 2004a). As a
result, an outbreak investigation was implemented in
the Sahrawi refugee camps in May 2010 and followed
up in October 2010 with the objective of confirming
the suspicion of PPRV circulation. This paper presents
the first report of PPRV lineage 4 circulation in Algeria.
Materials and Methods
Study area
The Sahrawi community
Sahrawi, literally ‘people from the desert’, are nomadic
and pastoral tribes who inhabited the Western Sahara
(Fig. 1) (Ramondino, 1997; Broglia and Volpato, 2008).
In 1975, as a consequence of the military occupation of
Western Sahara by Mauritanian and Moroccan military
forces, about 70 000 Sahrawi fled into Algeria (Spiegel
and Qassim, 2003; Loewenberg, 2005) where they gathered in refugee camps in the Tindouf province. Subsequently, a long political process led to the establishment
of the Sahrawi Arab Democratic Republic (SADR). Beside
the refugees camps, the SADR has also political control
over the eastern part of Western Sahara (the so called
‘liberated territories’ or ‘free zone’), which was liberated
from Moroccan occupation through guerrilla fighting.
The western portion of the Western Sahara is under
Moroccan control and is referred as Moroccan Southern
Province, separated from the ‘liberated territories’ by an
earthen wall (the ‘Berm’) and protected by land mines
ª 2011 Blackwell Verlag GmbH • Transboundary and Emerging Diseases.
M. De Nardi et al.
Fig. 1. Western Sahara and Sahrawi refugee camps in western Algeria.
(San Martı́n, 2004; Loewenberg, 2005; Broglia and Volpato, 2008). Overall, the Sahrawi territories encompass the
refugee camps and the liberated territories in Western
Sahara.
Since 1975, the Sahrawi people have lived as refugees
in camps (El Aaiun, Awserd, Smara, Dakhla, 27 Febrero
Peste des Petits Ruminants, Algeria
and Rabouni) which are located in the desert plateau of
Hamada in close proximity to the Algerian town of Tindouf, in the Tindouf province (Fig. 2). The closest camps
are located at a distance ranging between 15 and 50 km
from Tindouf; the distance between the six camps is variable, spanning from a minimum of 12 km (Rabouni-27
Febrero) to a maximum of about 160 km (Rabouni-Dakhla). The camps currently host about 165 000 people
whose livelihood (in terms of trade and source of proteins) relies primarily on the livestock kept within the
camps. Livestock breeding represents one of the main
income generating activities for Sahrawi. About 60 000
sheep and goats and 2000 camels are reared in semiintensive conditions in the camps: animals move freely
during the day, but are kept in rudimental holdings during the night. Small ruminants normally do not move
between camps. Semi-nomadic pastoralism is also practiced: livestock keepers in the camps move to grazing
areas within the liberated territories in Western Sahara
during times of low rainfall (September/October and
March/April). Transhumance for grazing purposes is
important to fatten animals and to increase the size of
the herd/flock before returning to the camps. In addition,
these semi-nomadic practices allow Sahrawi tribes to preserve their nomadic traditions and cultures (Broglia and
Volpato, 2008).
The Sahrawi Veterinary Services (SVS), under the
framework of the SADR Ministry of Public Health and in
collaboration with the Algerian veterinary authorities,
Fig. 2. Study area: Sahrawi refugee camps in the Tindouf province, western Algeria. Note: Map not to scale. Map generated using ArcGISTM 9.2
(ESRI, Redlands, CA, USA).
ª 2011 Blackwell Verlag GmbH • Transboundary and Emerging Diseases.
3
Peste des Petits Ruminants, Algeria
despite being still embryonic, makes huge efforts to perform animal health surveillance and to carry out disease
control in the Sahrawi territories. The surveillance system
currently in place relies predominantly on the recording
of livestock mortality rates and on clinical inspections at
the frontier posts and at the check points close to the
camps. Surveillance strategies and contingency plans for
the control of major transboundary animal diseases
(TADs) have not been developed and only basic laboratory facilities are available.
Data on livestock mortality events
A database with livestock mortality events reported in
the refugee camps since April 2009 was provided by the
SVS. The database was cleaned; and the mean of mortality events in the periods between April and December
2009, January and May 2010, and June and August 2010
was estimated. The recording of the mortality rates is
being implemented by SVS in collaboration and under
the coordination of the international Non-Governmental
Organization (NGO) ‘Movimiento por la Paz, el Desarme y la Libertad’ funded by the Spanish Cooperation.
Carcasses of livestock are routinely collected from the
camps to be adequately disposed of. This system, primarily established to improve the hygienic condition
within the camps, also guarantees the efficient recording
of mortality events in the livestock population and represents, therefore, an ‘embryonic’ early warning system
to detect unusual events. A strong deviation from the
average mortality rate normally triggers further investigations.
Survey area
In May 2010, SVS were still issuing, although at reducing
levels, reports of small ruminant deaths in the camps of
Smara, Awserd, Rabouni and El Aaiun. A targeted survey
was therefore implemented in Smara, Rabouni and Awserd in May 2010 with the aim of sampling diseased animals, as per case definition, to confirm the PPRV
circulation. The target population was sheep and goats
reared within the camps, and the study population was
represented by diseased animals. All field activities were
supported by SVS and the ‘Africa ‘70’ International NGO.
Case definition
A clinical suspicion of PPR was based on the identification of animals presenting at least two of the following
clinical signs: high fever (>41C, with inappetence and
marked depression), signs of pneumonia (respiratory distress and/or coughing), nasal and/or ocular discharges
(serous or mucopurulent discharges), mouth lesions
(necrotic foci and erosions) and diarrhoea. The PPRV
4
M. De Nardi et al.
infection was confirmed by laboratory diagnosis using
real-time and conventional RT-PCR in the World Reference Laboratory for PPR, Institute for Animal Health,
Pirbright, UK. The location of suspected cases of PPR
within the targeted camps relied on the SVS reports and
interviews with pastoralists.
Sampling strategy
The sample size (n) was based on the 2007 census population data (MoPH, 2007) and was calculated to achieve a
0.95 probability (P) of detecting at least one positive case
in the sample assuming an expected prevalence (d) of
30% and an infinite (N) population size (Thrusfield,
2007) as:
1
d
n ¼ ½1 ð1 PÞd ½ðN Þ þ 1
2
The specificity and sensitivity of the real-time and conventional RT-PCR have been assumed to be equal to
100%.
The prevalence was expected to be as high as 30%
based on results of a country-wide cross-sectional survey
implemented in 2008, which confirmed the presence of
antibodies against PPRV throughout the whole region in
28.3% of the sampled animals. In some provinces, seroprevalence was >40% (Di Nardo A, Rossi D, Lamin Saleh
S.M, Lejlifa S.M, Hamdi S.J, Sabatini M, Teodori L,
Savini G, Thrusfield M.V, unpublished observation).
Laboratory testing
Samples collected were oral, ocular and nasal swabs, and
whole unclotted blood (in EDTA). Samples were kept
refrigerated at +4C during collection procedures and
until shipment to the laboratory. All samples were dispatched to the World Reference Laboratory for PPR,
Institute for Animal Health, Pirbright (UK), where the
initial screening was performed by real-time RT-PCR
(Batten et al., 2011) and positive samples were confirmed
by conventional RT-PCR assay using a set of primers specific for the F gene of the PPRV. Briefly, RNA was
extracted from 1/10 tissue suspensions through the Universal (Qiagen, Crawley, UK) extraction robot using the
‘One for All’ protocol. RNA was then used as template in
real-time RT-PCR (Batten et al., 2011).
Sequencing and phylogenetic analysis
Sequence analysis of the F gene was performed on PCRpositive samples to identify the genetic lineage of the
virus. The evolutionary history was investigated using the
neighbour-joining method with distance matrices being
ª 2011 Blackwell Verlag GmbH • Transboundary and Emerging Diseases.
M. De Nardi et al.
computed using the Kimura 2-parameter nucleotide substitution model, as implemented in the software MEGA
5.05 (Tamura et al., 2011). The robustness of the tree
typology was assessed using 1000 bootstrap replicates.
Peste des Petits Ruminants, Algeria
between the refugee camps and the grazing areas, were
identified and interviewed; data on unusual disease and
mortality events were recorded.
Results
Epidemiological data collection
Supplementary epidemiological data (such as animals age
and sex, flock structure in term of species and breed, geographical origin of the flock, flock movement patterns,
recent introduction of new animals in the flock) and clinical signs were collected at the time of the survey through
semi-structured interviews conducted with animal owners
and clinical inspection of suspected animals. For this purpose, a specific questionnaire was developed and an ad
hoc database was created in Excel 2007 (Microsoft Corporation, Redmont, WA, USA).
Statistical analysis
The chosen statistical approach reflects the small number
of sampled animals.
For each refugee camp, the mean of deaths in the periods
April–December 2009 and June–August 2010 were compared with the mean of deaths in the January–May 2010
period by using the Student’s t-test (considering unequal
standard deviations) and the one-way analysis of variance
(when comparing simultaneously the means for the three
periods). In the latter, the assumption of similar population standard deviations was assessed by the Bartlett’s Test.
(Kirkwood and Sterne, 2003). The calculation of the Confidence Intervals for the mean was based on the t-distribution, whereas the calculation of exact Confidence Intervals
for proportion was based on probabilities derived from the
binomial distribution (Dohoo et al., 2010).
Univariable analysis was performed using the Fisher’s
exact test to identify potential risk factors and clinical
signs associated to PPR cases and to investigate the
association between clinical signs identified in PPR
positive and, overall, in sampled animals. Statistical
analysis and the design of the graph were performed in
Stata 10.1 SE (StataCorp LP, College Station, TX,
USA). A statistically significant threshold was set at a
P-value of 0.05. A P-value >0.05 and <0.10 was considered indicative of a weak association.
Participatory survey
A retrospective participatory survey was conducted in
October 2010, with the objective of investigating the
health of the livestock population in the grazing areas of
Western Sahara between November 2009 and May 2010.
Pastoralists, among those who practise transhumance
ª 2011 Blackwell Verlag GmbH • Transboundary and Emerging Diseases.
Livestock mortality within the refugee camps in the period April 2009–August 2010
In Awserd, El Aaiun and Smara, with estimated small
ruminant populations of respectively 13 800, 19 700 and
19 600 units (MoPH, 2007), the death toll was remarkably high and statistically significant differences were
found when the mean of deaths in the periods April–
December 2009 and June–August 2010 were compared
with the mean of deaths in the January–May 2010 period
(Fig. 3). Authorities reported that in Awserd, on average,
142 deaths (95%CI 107.6–176.1) in the period April–
December 2009, 642 (95%CI 447.2 – 836.0) in January–
May 2010 (P = 0.003) and 195 deaths in the period
June–August 2010 (P = 0.009) had occurred; in El Aaiun,
during the same time periods, the average reported deaths
were respectively 206 (95%CI 141.7–269.2), 982 (95%CI
657.5–1305.5) and 218 (P = 0.000); in Smara, data for
the first period were not available but the average
reported deaths in January–May 2010 and June–August
2010 were respectively 690 (95%CI 287.0–1093.7) and 266
(95%CI 13.4–517.9) (P = 0.01). Owing to the relatively
small number of observations collected in Awserd and El
Aaiun in the period June–August 2010, the Confidence
Intervals were not computed as they were not informative.
Survey data and laboratory analysis
Considering the expected prevalence and the sampling
strategy, it was necessary to sample nine animals to detect
at least one positive case with a 95% certainty. However,
to increase the chance of detecting the PPRV circulation
in a timely and cost-effective manner, only suspected animals (as per case definition) were sampled and more than
one diagnostic sample was taken from each animal.
In Smara, Rabouni and Awserd, a total of 21 samples
(four ocular swabs, seven nasal swabs, three oral swabs
and seven whole blood samples) were collected from nine
animals (eight sheep and one goat) suspected of having
been infected with PPRV. The real-time and conventional
RT-PCR test conducted on swabs and whole blood
detected the presence of PPRV genetic material in two
sheep and one goat reared respectively in Smara and
Awserd, confirming the circulation of the virus in the refugee camps. With reference to the samples, seven of 21
samples tested positive (three nasal swabs, two ocular
swabs and two whole blood). The two PPR-positive sheep
were purchased in Mauritania and then brought to the
5
Peste des Petits Ruminants, Algeria
M. De Nardi et al.
Fig. 3. Means of number of deaths recorded in the small ruminant populations of Awserd, El Aaiun and Smara camps in the period between
April 2009 and August 2010.
Smara livestock market; the PPR-positive goat was purchased in the Zemur location (Western Sahara) and
moved into the Awserd camp.
According to the livestock owners, the flocks from
which the positive animals originated had resided in
Mauritania and Western Sahara for the previous
12 months, during which time the flocks were not moved
from the origin villages. Both sheep were kept in a small
flock (five sheep) and no mortality events were recorded
in the previous 2 weeks, whereas the goat was part of a
larger mixed flock (20 sheep and 25 goats) with a history
of about 20 deaths in the previous 2 weeks. No statistical
association between animal status (PPR positive or negative) and selected variables such as species (P = 0.33), age
(P = 1.00) and origin and/or location of the flock in the
previous 12 months (P = 0.21) was detected. Furthermore, no animals were introduced in the original flocks
in that same period.
The clinical picture observed during the inspection
reflected a very generalized clinical situation. Clinical
signs detected in the PPR-positive animals are shown in
Table 1. With the exception of nasal discharge, no other
clinical signs were common within positive animals and
PPRV infections were only weakly associated with signs
of emaciation (P = 0.083). No mouth lesions were
detected in any of the positive animals.
Most of the sampled animals (Table 2) presented nasal
discharge (77.8%) varying from serous to muco-purulent,
fever (up to 41.5C) and depression (77.8%) and respiratory syndrome with dyspnoea and/or hyperpnoea
6
Table 1. Clinical signs detected in PPR-positive cases
Clinical signs
Sheep 1
Sheep 2
Goat
Nasal discharge
Fever/depression
Respiratory signs
Eye discharge
Diarrhoea
Buccal exudates/foam
Emaciation
Cough
Oral erosion
Yes
Yes
Yes
Yes
No
No
Yes
No
No
Yes
Yes
No
Yes
No
No
No
Yes
No
Yes
No
No
No
Yes
No
Yes
No
No
Table 2. Clinical signs identified in all sampled animals
Clinical signs
No of animals
with clinical sign/Tot
animal sampled (%)
Exact 95%
confidence intervals
Nasal discharge
Fever/depression
Respiratory signs
Eye discharge
Diarrhoea
Buccal exudates/foam
Emaciation
Cough
Oral erosion
7/9
7/9
6/9
3/9
3/9
3/9
2/9
1/9
0/9
39.9–97.2
39.9–97.2
29.9–92.5
7.5–70.0
7.5–70.0
7.5–70.0
2.8–60.0
0.3–48.2
–
(77.8)
(77.8)
(66.7)
(33.3)
(33.3)
(33.3)
(22.2)
(11.1)
(0.0)
(66.7%). Few animals showed mucous ocular discharge
(33.3%), diarrhoea (33.3%), cough (11.1%) and signs of
emaciations (22.2%). One-third of the animals (33.3%)
ª 2011 Blackwell Verlag GmbH • Transboundary and Emerging Diseases.
M. De Nardi et al.
Peste des Petits Ruminants, Algeria
Fig. 4 Midpoint-rooted neighbour-joining tree showing the phylogenetic relationship of peste des petits ruminants virus (PPRV) F gene isolates.
Samples R15-10/14, R15-10/16 and R15-10/18 correspond to the PPRV-positive samples collected from animals in the Sahrawi refugee camps.
presented oral exudates and/or foam, but none of the
sampled animals presented oral lesions. Most of the animals with fever and depression (7/9) were also affected by
respiratory signs (P = 0.083) but only one had diarrhoea
(P = 0.083).
Sequencing of the viral F gene performed on samples
from positive animals indicated that the PPRV belonged
to lineage IV. Neighbour-joining analysis indicated a
99.3% percentage of identity with the PPRV isolated in
Morocco in 2008–09 (Fig. 4).
Participatory appraisal
The retrospective participatory survey showed an unusual
increase in mortality in small ruminant flocks kept in the
grazing areas of the Western Sahara in the period December 2009–April 2010. Of 29 interviewed pastoralists,
10.3% (3/29) reported a mortality rate of ‡50% among
their animals (reaching a peak of 70% in one case),
48.3% (14/29) pastoralists reported rates between 20%
ª 2011 Blackwell Verlag GmbH • Transboundary and Emerging Diseases.
and 49% while 41.4% (12/29) pastoralists recorded rates
of <20%. Although it was not possible to substantiate
these data through field investigations and laboratory
analysis, they seemed to be indicative of an unusual situation consistent with the outbreak of an infectious disease
such as PPR.
Discussion
The survey implemented in the Sahrawi refugee camps
(western Algeria) in May 2010 resulted in the detection of
PPRV genetic material in three of nine sampled animals.
Despite the recently reported serological evidence for PPR
circulation in different regions of Algeria, this is the first
time that the presence of the PPRV has been confirmed
to be circulating in Algeria. Molecular typing and phylogenetic analysis characterized the strain discovered as
belonging to lineage IV, a lineage that is widespread
across the Arabian Peninsula, in southern Asia, in the
Middle East and recently across different African coun7
Peste des Petits Ruminants, Algeria
tries (Banyard et al., 2010; Khalafalla et al., 2010). The
phylogenetic analysis indicated a close relationship with
the PPRV isolated during the Moroccan PPR outbreak in
2008. To notify the OIE of the first evidence of PPRV circulation in Algeria and the identification of the genetic
lineage, the Director of the Sahrawi Veterinary Services
communicated these findings to the Director of the Algerian Veterinary Services in August 2010.
The origin of the outbreak remains unknown despite
evidence from field data collected suggesting that the
virus could have been introduced into the refugee camps
in November 2009 following the importation of small
ruminants from Mauritania and the liberated territories
of Western Sahara for the celebration of the Aid al Adha
festivity (Islamic Easter, end of November 2009). Alternatively, animals could have been illegally moved directly
from Morocco or from the Moroccan Southern Province
into Algeria (S.M. Lamin Saleh, personal communication). Owing to the high demand of meat in the camps,
the amount of animals raised is not sufficient to satisfy
the protein needs of the population. For this reason, there
is a flourishing livestock trade bringing animals into the
camps. Animal traders usually buy goats and sheep in
Mauritania, Algeria, Mali or in the liberated territories
and sell the animals in the livestock markets located in
the refugee camps. Islamic festivities result in an increase
in animal trade from neighbouring countries. For example, the Aid Al Adha festivity is celebrated by each family
by slaughtering a ram and, as a consequence, thousands
of animals are purchased and then trucked to the camps
and sold in the livestock markets. In 2009, more than
7000 sheep were traded from Mauritania and Western
Sahara (MoPH, 2009). Refugee camps do not only represent the final trade destination: small ruminants and camels are also exported to other destinations such as the
town of Tindouf and sometimes into northern Algeria.
Therefore, the refugee camps represent also a trade hub
where animals are imported from neighbouring countries,
sold to traders in the livestock markets in the camps and
finally transported to other destinations. The recent evidence for a high seroprevalence of PPR in the Tindouf
province (OIE, 2011b) may be linked to this trade network.
The high percentage of animals detected with antibodies against the PPRV (as the 2005 and 2008 surveys indicate) and the presence of local breeds of sheep and goats
might have contributed to the sub-acute and, probably,
to the sub-clinical spread of the virus within the camps
and in the Sahrawi territories. Indeed, only generalized,
non-specific clinical signs were detected in PPR-positive
animals hardly referable only to PPR infection. This is
not unusual as PPR infections are often confused and
exacerbated by secondary infections including, among
8
M. De Nardi et al.
others, pasteurelossis, contagious ecthyma, contagious
caprine pleuropneumonia and bluetongue (Rossiter,
2004a; Couacy-Hymann et al., 2005; Diallo et al., 2007).
In the Sahrawi territories, factors such as the onset of the
cold season (January–February) associated with the emergence of secondary infections might have thereafter contributed to an increase in the mortality rates recorded
between January and May 2010. Climatic stresses are
well-documented triggering factors for PPR (Rossiter,
2004a).
As indicated by the mortality rates in the period June–
August 2010, the spread of disease since June 2010
appeared to be drastically reduced in the camps: the
reduction of the susceptible population, in a rather closed
environment such as the camps, has presumably contributed to limiting the spread of the disease. In fact, the
majority of the livestock trade occurs in specific periods
but, overall, animals are only sporadically moved out of
and between the camps during the year. As a consequence, the susceptible animal population present in late
May was probably too small to efficiently maintain the
virus circulation.
Although the disease appeared to be self-limiting, the
risk of further re-introduction into the camps from
affected regions and the dissemination to other free areas
should not be underestimated. A contingency plan based
on enhanced surveillance and preventive vaccination of
small ruminants was therefore promoted to control the
disease and to prevent the occurrence of new outbreaks.
Acknowledgements
The authors would like to thank the personnel of the
Sahrawi Veterinary Services for providing invaluable contributions to the study, the Italian Society for Tropical
Veterinary and International Cooperation (SIVTRO) and
the International NGO ‘Africa ‘70’ for the logistics. The
study was implemented under the framework of the
‘Soutien à l’élevage de bétail dans les camps de réfugiés
Sahraouis’ project (ONG-PVD/2006/131-812) coordinated
by Africa ‘70.
References
Anderson, E.C., 1995: Morbilliviruses in wildlife (in relation to
their population biology and disease control in domestic
animals). Vet. Microbiol. 44, 319–332.
Banyard, A.C., S. Parida, C. Batten, C. Oura, O. Kwiatek, and
G. Libeau, 2010: Global distribution of peste des petits
ruminants virus and prospects for improved diagnosis and
control. J. Gen. Virol. 91, 2885–2897.
Batten, C.A., A.C. Banyard, D.P. King, M.R. Henstock, L.
Edwards, A. Sanders, H. Buczkowski, C.C. Oura, and
ª 2011 Blackwell Verlag GmbH • Transboundary and Emerging Diseases.
M. De Nardi et al.
T. Barret, 2011: A real time RT-PCR assay for the specific
detection of peste des petits ruminants virus. J. Virol. Methods 171, 401–404.
Broglia, A., and G. Volpato, 2008: Pastoralism and displacement: strategies and limitations in livestock raising by Sahrawi refugees after thirty years of exile. J. Agr. Environ. Int.
Dev. 102, 105–122.
Centre for Food Security and Public Health (CFSPH) 2008:
Peste des petits ruminants. Available at http://www.cfsph.iastate.edu/DiseaseInfo/disease.php?name=peste-des-petitsruminants&lang=en (accessed April 19, 2011).
Couacy-Hymann, E., C. Bodjo, T. Danho, G. Libeau, and A.
Diallo, 2005: Surveillance of wildlife as a tool for monitoring
rinderpest and peste des petits ruminants in West Africa.
Rev. Sci. Tech. 24, 869–877.
Diallo, A., C. Minet, C. Le Goff, G. Berhe, E. Albina, G. Libeau, and T. Barrett, 2007: The threat of peste des petits
ruminants: progress in vaccine development for disease control. Vaccine 25, 5591–5597.
Dohoo, I., W. Martin, and H. Stryhn, 2010: Veterinary Epidemiologic Research, 2nd edn. VER Inc., Charlottetown, Canada.
Food and Agriculture Organization of the United Nations
(FAO) 2008: Peste des petites ruminants (PPR) in Morocco.
EMPRES Watch. Available at http://www.fao.org/fileadmin/
user_upload/newsroom/docs/aj120e00.pdf (accessed April
19, 2011).
Food and Agriculture Organization of the United Nations
(FAO) 2009: Peste des petits ruminants: an increasing threat
to small ruminant production in Africa and Asia. EMPRES
Transboundary Animal Disease Bullettin No. 33. Available
at ftp://ftp.fao.org/docrep/fao/011/i0919e/i0919e00.pdf
(accessed April 19, 2011).
Kaukarbayevich, K.Z., 2009: Epizootological analysis of PPR
spread in African continent and in Asia countries. Afr. J.
Agr. Res. 4, 787–790.
Khalafalla, A.I., I.K. Saeed, Y.H. Ali, M.B. Abdurrahman, O.
Kwiatek, G. Libeau, A.A. Obeida, and Z. Abbas, 2010: An
outbreak of peste des petits ruminants (PPR) in camels in
the Sudan. Acta Trop. 116, 161–165.
Kirkwood, B.R., and A.C. Sterne, 2003: Essential Medical Statistics, 2nd edn. Blackwell Science Ltd., Oxford, UK.
ª 2011 Blackwell Verlag GmbH • Transboundary and Emerging Diseases.
Peste des Petits Ruminants, Algeria
Loewenberg, S., 2005: Displacement is permanent for the Sahrawi refugees. Lancet 365, 1295–1296.
Ministry of Public Health (MoPH) 2007: Animal Census,
2007.National Veterinary Department, Ministry of Public
Health, Sahrawi Arab Democratic Republic, Rabouni, Algeria.
Ministry of Public Health (MoPH) 2009: Livestock Trade Statistics, 2007–09. National Veterinary Department, Ministry
of Public Health, Sahrawi Arab Democratic Republic, Rabouni, Algeria.
Ministry of Public Health (MoPH) 2010: Animal Mortality
Statistics, 2009–10. National Veterinary Department, Ministry of Public Health, Sahrawi Arab Democratic Republic,
Rabouni, Algeria.
Ramondino, F., 1997: Polisario, un Astronave Dimenticata nel
Deserto. Gamberetti, Rome.
Rossiter, P.B., 2004a: Peste des petits ruminants. In: Coetzer,
J.A.W. and R.C. Tustin (eds), Infectious Disease of Livestock,
2nd edn, pp. 660–672. Oxford University Press, South
Africa.
Rossiter, P.B., 2004b: Rinderpest. In: Coetzer, J.A.W. and R.C.
Tustin (eds), Infectious Disease of Livestock, 2nd edn, pp.
629–659. Oxford University Press, South Africa.
San Martı́n, P., 2004: Briefing: Western Sahara: road to perdition? Afr. Aff. 103, 651–660.
Spiegel, P.B., and M. Qassim, 2003: Forgotten refugees and
other displaced populations. Lancet 362, 72–74.
Tamura, K., D. Peterson, N. Peterson, G. Stecher, M. Nei, and
S. Kumar, 2011: MEGA5: molecular evolutionary genetics
analysis using maximum likelihood, evolutionary distance,
and maximum parsimony methods. Mol. Biol. Evol.
PMID:21546353. doi: 10.1093/molbev/msr121.
Thrusfield, M.V., 2007: Veterinary Epidemiology, 3rd revised
edn. Blackwell Science Ltd., Oxford, UK.
World Organization for Animal Health (OIE) 2011a: World
Animal Health Information Database (WAHID) – Version:
1.4. Available at http://web.oie.int/wahis/public.php?page=
home (accessed April 19, 2011).
World Organization for Animal Health (OIE) 2011b: Immediate Notification Report. Ref OIE: 10384, Report Date: 20/03/
2011, Country: Algeria.
9