Combining viral genetic and animal mobility network data to unravel peste des petits ruminants transmission dynamics in West Africa.

Peste des petits ruminants (PPR) is a deadly viral disease that mainly affects small domestic ruminants. This disease threaten global food security and rural economy but its control is complicated notably because of extensive, poorly monitored animal movements in infected regions. Here we combined the largest PPR virus genetic and animal mobility network data ever collected in a single region to improve our understanding of PPR endemic transmission dynamics in West African countries. Phylogenetic analyses identified the presence of multiple PPRV genetic clades that may be considered as part of different transmission networks evolving in parallel in West Africa. A strong correlation was found between virus genetic distance and network-related distances. Viruses sampled within the same mobility communities are significantly more likely to belong to the same genetic clade. These results provide evidence for the importance of animal mobility in PPR transmission in the region. Some nodes of the network were associated with PPRV sequences belonging to different clades, representing potential "hotspots" for PPR circulation. Our results suggest that combining genetic and mobility network data could help identifying sites that are key for virus entrance and spread in specific areas. Such information could enhance our capacity to develop locally adapted control and surveillance strategies, using among other risk factors, information on animal mobility.

First Report of the Emergence of Peste des Petits Ruminants Lineage IV Virus in Senegal.

Peste des petits ruminants (PPR) is a highly contagious viral disease and one of the deadliest affecting wild goats, sheep, and small ruminants; however, goats are generally more sensitive. The causative agent is the Peste des Petits Ruminants virus (PPRV), which is a single-stranded RNA virus of negative polarity belonging to the Paramyxoviridae family. In February 2020, an active outbreak of PPR was reported in a herd of a transhumant farmer in the village of Gainth Pathé (department of Kounguel, Kaffrine region, Senegal). Of the ten swabs collected from the goats, eight returned a positive result through a quantitative real-time PCR. The sample that yielded the strongest signal from the quantitative real-time PCR was further analyzed with a conventional PCR amplification and direct amplicon sequencing. A phylogenetic analysis showed that the sequence of the PPR virus obtained belonged to lineage IV. These results confirm those found in the countries bordering Senegal and reinforce the hypothesis of the importance of animal mobility between these neighboring countries in the control of PPRV. In perspective, following the discovery of this lineage IV in Senegal, a study on its dispersion is underway throughout the national territory. The results that will emerge from this study, associated with detailed data on animal movements and epidemiological data, will provide appropriate and effective information to improve PPR surveillance and control strategies with a view to its eradication.

Comparative evolutionary analyses of peste des petits ruminants virus genetic lineages.

Peste des petits ruminants virus (PPRV) causes a highly infectious disease affecting mainly goats and sheep in large parts of Africa, Asia, and the Middle East and has an important impact on the global economy and food security. Full genome sequencing of PPRV strains has proved to be critical to increasing our understanding of PPR epidemiology and to inform the ongoing global efforts for its eradication. However, the number of full PPRV genomes published is still limited and with a heavy bias towards recent samples and genetic Lineage IV (LIV), which is only one of the four existing PPRV lineages. Here, we generated genome sequences for twenty-five recent (2010-6) and seven historical (1972-99) PPRV samples, focusing mainly on Lineage II (LII) in West Africa. This provided the first opportunity to compare the evolutionary pressures and history between the globally dominant PPRV genetic LIV and LII, which is endemic in West Africa. Phylogenomic analysis showed that the relationship between PPRV LII strains was complex and supported the extensive transboundary circulation of the virus within West Africa. In contrast, LIV sequences were clearly separated per region, with strains from West and Central Africa branched as a sister clade to all other LIV sequences, suggesting that this lineage also has an African origin. Estimates of the time to the most recent common ancestor place the divergence of modern LII and LIV strains in the 1960s-80s, suggesting that this period was particularly important for the diversification and spread of PPRV globally. Phylogenetic relationships among historical samples from LI, LII, and LIII and with more recent samples point towards a high genetic diversity for all these lineages in Africa until the 1970s-80s and possible bottleneck events shaping PPRV's evolution during this period. Molecular evolution analyses show that strains belonging to LII and LIV have evolved under different selection pressures. Differences in codon usage and adaptative selection pressures were observed in all viral genes between the two lineages. Our results confirm that comparative genomic analyses can provide new insights into PPRV's evolutionary history and molecular epidemiology. However, PPRV genome sequencing efforts must be ramped up to increase the resolution of such studies for their use in the development of efficient PPR control and surveillance strategies.

A Phylogeographic Analysis of Porcine Parvovirus 1 in Africa.

Porcine parvovirus 1 (PPV1) is recognized as a major cause of reproductive failure in pigs, leading to several clinical outcomes globally known as SMEDI. Despite being known since the late 1960s its circulation is still of relevance to swine producers. Additionally, the emergence of variants such as the virulent 27a strain, for which lower protection induced by vaccines has been demonstrated, is of increasing concern. Even though constant monitoring of PPV1 using molecular epidemiological approaches is of pivotal importance, viral sequence data are scarce especially in low-income countries. To fill this gap, a collection of 71 partial VP2 sequences originating from eight African countries (Burkina Faso, Côte d'Ivoire, Kenya, Mozambique, Namibia, Nigeria, Senegal, and Tanzania) during the period 2011-2021 were analyzed within the context of global PPV1 variability. The observed pattern largely reflected what has been observed in high-income regions, i.e., 27a-like strains were more frequently detected than less virulent NADL-8-like strains. A phylogeographic analysis supported this observation, highlighting that the African scenario has been largely shaped by multiple PPV1 importation events from other continents, especially Europe and Asia. The existence of such an international movement coupled with the circulation of potential vaccine-escape variants requires the careful evaluation of the control strategies to prevent new strain introduction and persistence.

Insight on Bluetongue virus transmission in small ruminants in Senegal.

Bluetongue (BT) is an infectious, arthropod-borne viral disease of domestic and wild ruminants. The disease causes animal mortality, production decrease and commercial limits for herds. Despite the active circulation of the disease in the world, few studies have been carried out in Senegal. The objective of this study was to assess the current prevalence of BT in small ruminants and the serotypes circulating in Senegal. A cross-sectional study was conducted in the fourteen regions of Senegal. After the sampling campaign, sera collected in sheep and goats herds were screened for the presence of Bluetongue virus (BTV) specific antibodies using c-Elisa. The whole blood of seropositive animals was further analyzed by RT-qPCR and positive samples were typed to identify BTV serotypes. Analysis of several risk factors such as age, sex and species of animals was performed using logistic regression. The overall seroprevalence of BTV in Senegal was 72.6% (95% CI: 70.3-74.9%) with 75.9% (95% CI: 72.2-79.5%) in goat and 70.6% (95% CI: 67.5-73.6%) in sheep. Female (prevalence=77.1%) and adult (prevalence=80%) animals showed the highest seropositivity to BTV compared respectively to male (55.7%, p=6.133e-09) and young (49.4%, p < 2.2e-16). The RT-qPCR results showed the presence of BT viral genome in 359 small ruminants. The results obtained from serological and genotyping studies showed an active spread of the Bluetongue virus in domestic ruminants and phylogenetic analysis showed that the BTV-2 is one of the circulating serotypes in Senegal. This study allows having baseline information for controlling Bluetongue in Senegal.

Burden of anemia and intestinal parasites in farmers and family members and owned livestock in two geographic locations in Senegal before and during the rainy seasons.

Different environmental conditions can impact the burden of anemia and intestinal parasite infections in human and livestock populations. The objective of this study was to compare the prevalence of anemia and intestinal parasite infections in farmers, family members, and owned sheep in two geographic locations along the Senegal River in June (end of the dry season) and September (rainy season). In Diawara, the prevalence of anemia in humans was high in June (74%) and remained high in September (75%) (p = 0.91). The prevalence of intestinal parasite infections increased from 7% in June to 54% in September (p < 0.05). Anemia was associated with age (children) and sex (women) (p < 0.05); but not with a positive diagnosis of intestinal parasite infection (p = 0.73). In sheep, the prevalence of anemia increased from 43% in June to 73% in September (p < 0.05), and the prevalence of intestinal parasite infections increased from 75% in June to 100% in September (p < 0.05). A positive diagnosis of Haemonchus contortus was associated with anemia (p = 0.05) and loss of body weight (2.4 kg) (p = 0.08). In Mpal, similar anemia and parasite infection trends were observed in children and sheep. The persistent high prevalence of anemia, and the impact of the rainy season on the burden of intestinal parasite infections in farmers, family members, and owned sheep can justify a One Health approach, where Senegal's ministries of health and of agriculture share resources for implementation and evaluation of government program efforts to reduce anemia in children and women, as well as morbidity and mortality in owned livestock; particularly in remote areas where public health services and veterinary services are very limited.

Identification of drivers of Rift Valley fever after the 2013-14 outbreak in Senegal using serological data in small ruminants.

Rift Valley fever (RVF) is a mosquito-borne disease mostly affecting wild and domestic ruminants. It is widespread in Africa, with spillovers in the Arab Peninsula and the southwestern Indian Ocean. Although RVF has been circulating in West Africa for more than 30 years, its epidemiology is still not clearly understood. In 2013, an RVF outbreak hit Senegal in new areas that weren't ever affected before. To assess the extent of the spread of RVF virus, a national serological survey was implemented in young small ruminants (6-18 months old), between November 2014 and January 2015 (after the rainy season) in 139 villages. Additionally, the drivers of this spread were identified. For this purpose, we used a beta-binomial ([Formula: see text]) logistic regression model. An Integrated Nested Laplace Approximation (INLA) approach was used to fit the spatial model. Lower cumulative rainfall, and higher accessibility were both associated with a higher RVFV seroprevalence. The spatial patterns of fitted RVFV seroprevalence pointed densely populated areas of western Senegal as being at higher risk of RVFV infection in small ruminants than rural or southeastern areas. Thus, because slaughtering infected animals and processing their fresh meat is an important RVFV transmission route for humans, more human populations might have been exposed to RVFV during the 2013-2014 outbreak than in previous outbreaks in Senegal.

Porcine circovirus-2 in Africa: Identification of continent-specific clusters and evidence of independent viral introductions from Europe, North America and Asia.

Porcine circovirus-2 (PCV-2) is associated with several disease syndromes in domestic pigs that have a significant impact on global pig production and health. Currently, little is known about the status of PCV-2 in Africa. In this study, a total of 408 archived DNA samples collected from pigs in Burkina Faso, Cameroon, Cape Verde, Ethiopia, the Democratic Republic of the Congo, Mozambique, Nigeria, Senegal, Tanzania and Zambia between 2000 and 2018 were screened by PCR for the presence of PCV-2. Positive amplicons of the gene encoding the viral capsid protein (ORF2) were sequenced to determine the genotypes circulating in each country. Four of the nine currently known genotypes of PCV-2 were identified (i.e. PCV-2a, PCV-2b, PCV-2d and PCV-2 g) with more than one genotype being identified in Burkina Faso, Ethiopia, Nigeria, Mozambique, Senegal and Zambia. Additionally, a phylogeographic analysis which included 38 additional ORF2 gene sequences of PCV-2s previously identified in Mozambique, Namibia and South Africa from 2014 to 2016 and 2019 to 2020 and available in public databases, demonstrated the existence of several African-specific clusters and estimated the approximate time of introduction of PCV-2s into Africa from other continents. This is the first in-depth study of PCV-2 in Africa and it has important implications for pig production at both the small-holder and commercial farm level on the continent.

Unexpected Rift Valley fever outbreak, northern Mauritania.

During September-October 2010, an unprecedented outbreak of Rift Valley fever was reported in the northern Sahelian region of Mauritania after exceptionally heavy rainfall. Camels probably played a central role in the local amplification of the virus. We describe the main clinical signs (hemorrhagic fever, icterus, and nervous symptoms) observed during the outbreak.

Anemia and intestinal parasites in farmers and family members and sheep in two agro-ecological zones in Senegal.

The burden of anemia in Senegal is high, particularly in children and women in rural households. The main objectives of the study reported here were (i) to measure and compare the prevalence of anemia and intestinal parasitic infections in farmers and family members and sheep in two agro-ecological zones in Senegal and (ii) to examine the association between anemia and age or sex in farmers and family members. The study was conducted in Mpal (250 km from Dakar, the capital city) and Diawara (700 km from Dakar, a remote location near the Malian border). In humans, the prevalence of anemia was higher in Diawara (64/86 = 74%), compared to Mpal (13/29 = 45%) (p < 0.01). Using logistic regression, the odds of anemia were 20.3, 5.7, and 3.2 times higher in children 1-4 years old, children 5-12 years-old, and teenagers 13-19 years old, respectively, compared to adults 20-60 years old, after controlling for study site and sex (p < 0.05). In Diawara, the odds of anemia were 2.9 times higher in women, compared to men, after controlling for age (p = 0.06). The prevalence of intestinal parasites (Giardia sp.) was the same (7%) at both locations. In sheep, the prevalence of low packed cell volume (PCV) and low body condition was higher in Diawara (48/60 = 60% and 11/60 = 18%, respectively), compared to Mpal (23/46 = 50% and 0/46 = 0%, respectively) (p < 0.05). Clinical anemia was associated (p < 0.01) with low PCV and a positive diagnosis of H. contortus. Overall, the prevalence of anemia was higher in farmers and family members and owned sheep in Diawara. In addition, anemia was more common in children and women, an indication that intra-household food allocation may be regulated in favor of men and older age groups. The consequences of livestock affected with anemia and undernutrition can be significant. High morbidity and mortality in livestock can lead to low household income, inadequate household access to and individual consumption of animal source foods, and subsequent risk of anemia in children and women in rural households in Senegal.

Persistence of the historical lineage I of West Africa against the ongoing spread of the Asian lineage of peste des petits ruminants virus.

Peste des petits ruminants (PPR) is a highly contagious disease of small ruminants. The causal agent, PPR virus (PPRV), is classified into four genetically distinct lineages. Lineage IV, originally from Asia, has shown a unique capacity to spread across Asia, the Middle East and Africa. Recent studies have reported its presence in two West African countries: Nigeria and Niger. Animals are frequently exchanged between Mali and Niger, which could allow the virus to enter and progress in Mali and to other West African countries. Here, PPRV samples were collected from sick goats between 2014 and 2017 in both Mali and in Senegal, on the border with Mali. Partial PPRV nucleoprotein gene was sequenced to identify the genetic lineage of the strains. Our results showed that lineage IV was present in south-eastern Mali in 2017. This is currently the furthest West the lineage has been detected in West Africa. Surprisingly, we identified the persistence at least until 2014 of the supposedly extinct lineage I in two regions of Mali, Segou and Sikasso. Most PPRV sequences obtained in this study belonged to lineage II, which is dominant in West Africa. Phylogenetic analyses showed a close relationship between sequences obtained at the border between Senegal and Mali, supporting the hypothesis of an important movement of the virus between the two countries. Understanding the movement of animals between these countries, where the livestock trade is not fully controlled, is very important in the design of efficient control strategies to combat this devastating disease.

Transboundary spread of equine influenza viruses (H3N8) in West and Central Africa: Molecular characterization of identified viruses during outbreaks in Niger and Senegal, in 2019.

Since November 2018, several countries in West and Central Africa have reported mortalities in donkeys and horses. Specifically, more than 66,000 horses and donkeys have succumbed to disease in Burkina Faso, Chad, Cameroon, The Gambia, Ghana, Mali, Niger, Nigeria, and Senegal. Strangles caused by Streptococcus equi subsp equi, African Horse Sickness (AHS) virus, and Equine influenza virus (EIV) were all suspected as potential causative agents. This study reports the identification of EIV in field samples collected in Niger and Senegal. Phylogenetic analysis of the hemagglutinin and neuraminidase genes revealed that the identified viruses belonged to clade 1 of the Florida sublineage and were very similar to viruses identified in Nigeria in 2019. Interestingly, they were also more similar to EIVs from recent outbreaks in South America than to those in Europe and the USA. This is one of the first reports providing detailed description and characterization of EIVs in West and Central Africa region.

External quality assessment of Rift Valley fever diagnosis in countries at risk of the disease: African, Indian Ocean and Middle-East regions.

Rift Valley fever virus (RVFV), an arbovirus belonging to the Phlebovirus genus of the Phenuiviridae family, causes the zoonotic and mosquito-borne RVF. The virus, which primarily affects livestock (ruminants and camels) and humans, is at the origin of recent major outbreaks across the African continent (Mauritania, Libya, Sudan), and in the South-Western Indian Ocean (SWIO) islands (Mayotte). In order to be better prepared for upcoming outbreaks, to predict its introduction in RVFV unscathed countries, and to run efficient surveillance programmes, the priority is harmonising and improving the diagnostic capacity of endemic countries and/or countries considered to be at risk of RVF. A serological inter-laboratory proficiency test (PT) was implemented to assess the capacity of veterinary laboratories to detect antibodies against RVFV. A total of 18 laboratories in 13 countries in the Middle East, North Africa, South Africa, and the Indian Ocean participated in the initiative. Two commercial kits and two in-house serological assays for the detection of RVFV specific IgG antibodies were tested. Sixteen of the 18 participating laboratories (88.9%) used commercial kits, the analytical performance of test sensitivity and specificity based on the seroneutralisation test considered as the reference was 100%. The results obtained by the laboratories which used the in-house assay were correct in only one of the two criteria (either sensitivity or specificity). In conclusion, most of the laboratories performed well in detecting RVFV specific IgG antibodies and can therefore be considered to be prepared. Three laboratories in three countries need to improve their detection capacities. Our study demonstrates the importance of conducting regular proficiency tests to evaluate the level of preparedness of countries and of building a network of competent laboratories in terms of laboratory diagnosis to better face future emerging diseases in emergency conditions.

It's risky to wander in September: Modelling the epidemic potential of Rift Valley fever in a Sahelian setting.

Estimating the epidemic potential of vector-borne diseases, along with the relative contribution of underlying mechanisms, is crucial for animal and human health worldwide. In West African Sahel, several outbreaks of Rift Valley fever (RVF) have occurred over the last decades, but uncertainty remains about the conditions necessary to trigger these outbreaks. We use the basic reproduction number (R0) as a measure of RVF epidemic potential in northern Senegal, and map its value in two distinct ecosystems, namely the Ferlo and the Senegal River delta and valley. We consider three consecutive rainy seasons (July-November 2014, 2015 and 2016) and account for several vector and animal species. We parametrize our model with estimates of Aedes vexans arabiensis, Culex poicilipes, Culex tritaeniorhynchus, cattle, sheep and goat abundances. The impact of RVF virus introduction is assessed every week over northern Senegal. We highlight September as the period of highest epidemic potential in northern Senegal, resulting from distinct dynamics in the two study areas. Spatially, in the seasonal environment of the Ferlo, we observe that high-risk locations vary between years. We show that decreased vector densities do not greatly reduce R0 and that cattle immunity has a greater impact on reducing transmission than small ruminant immunity. The host preferences of vectors and the temperature-dependent time interval between their blood meals are crucial parameters needing further biological investigations.

Assessing the Risk of Occurrence of Bluetongue in Senegal.

Bluetongue is a non-contagious viral disease affecting small ruminants and cattle that can cause severe economic losses in the livestock sector. The virus is transmitted by certain species of the genus Culicoides and consequently, understanding their distribution is essential to enable the identification of high-risk transmission areas. In this work we use bioclimatic and environmental variables to predict vector abundance, and estimate spatial variations in the basic reproductive ratio  R0. The resulting estimates were combined with livestock mobility and serological data to assess the risk of Bluetongue outbreaks in Senegal. The results show an increasing abundance of C. imicola, C. oxystoma, C. enderleini, and C. miombo from north to south. R0 < 1 for most areas of Senegal, whilst southern (Casamance) and southeastern (Kedougou and part of Tambacounda) agro-pastoral areas have the highest risk of outbreak (R0 = 2.7 and 2.9, respectively). The next higher risk areas are in the Senegal River Valley (R0 = 1.07), and the Atlantic coast zones. Seroprevalence rates, shown by cELISA, weren't positively correlated with outbreak probability. Future works should include follow-up studies of competent vector abundancies and serological surveys based on the results of the risk analysis conducted here to optimize the national epidemiological surveillance system.

Rift Valley fever in northern Senegal: A modelling approach to analyse the processes underlying virus circulation recurrence.

Rift Valley fever (RVF) is endemic in northern Senegal, a Sahelian area characterized by a temporary pond network that drive both RVF mosquito population dynamics and nomadic herd movements. To investigate the mechanisms that explain RVF recurrent circulation, we modelled a realistic epidemiological system at the pond level integrating vector population dynamics, resident and nomadic ruminant herd population dynamics, and nomadic herd movements recorded in Younoufere area. To calibrate the model, serological surveys were performed in 2015-2016 on both resident and nomadic domestic herds in the same area. Mosquito population dynamics were obtained from a published model trained in the same region. Model comparison techniques were used to compare five different scenarios of virus introduction by nomadic herds associated or not with vertical transmission in Aedes vexans. Our serological results confirmed a long lasting RVF endemicity in resident herds (IgG seroprevalence rate of 15.3%, n = 222), and provided the first estimation of RVF IgG seroprevalence in nomadic herds in West Africa (12.4%, n = 660). Multivariate analysis of serological data suggested an amplification of the transmission cycle during the rainy season with a peak of circulation at the end of that season. The best scenario of virus introduction combined yearly introductions of RVFV from 2008 to 2015 (the study period) by nomadic herds, with a proportion of viraemic individuals predicted to be larger in animals arriving during the 2nd half of the rainy season (3.4%). This result is coherent with the IgM prevalence rate (4%) found in nomadic herds sampled during the 2nd half of the rainy season. Although the existence of a vertical transmission mechanism in Aedes cannot be ruled out, our model demonstrates that nomadic movements are sufficient to account for this endemic circulation in northern Senegal.

Application of exponential random graph models to determine nomadic herders' movements in Senegal.

Understanding human and animal mobility patterns is a key to predict local and global disease spread. We analysed the nomad herds' movement network in a pilot area of northern Senegal and used exponential random graph models (ERGM) to investigate the reasons behind these movements. We interviewed 132 nomadic herders to collect information about nomad herd structures, movements, and reasons for taking specific routes or gathering in certain areas. We constructed a spatially explicit network with villages as the nodes and nomad herds' movements as the connecting edges. The final ERGM showed that node and edge attributes such as presence of cattle in the herd (odds ratio = 12, CI: 5.3, 27.3), morbidity (odds ratio = 3.6, CI: 2.3, 5.7), and lack of water (odds ratio = 2, CI: 1.3, 3.1) were important predictors of nomad herds' movements. This study not only provides valuable information for monitoring important livestock diseases such as Rift Valley Fever in Senegal, but also helps implement outreach, education, and intervention programs for other emerging and endemic diseases affecting nomadic herds.

Corrigendum: Genetic Evidence for Transboundary Circulation of Peste Des Petits Ruminants Across West Africa.

[This corrects the article DOI: 10.3389/fvets.2019.00275.].

Genetic Evidence for Transboundary Circulation of Peste Des Petits Ruminants Across West Africa.

Peste des Petits Ruminants (PPR) is a viral disease affecting predominantly small ruminants. Due to its transboundary nature, regional coordination of control strategies will be key to the success of the on-going PPR eradication campaign. Here, we aimed at exploring the extent of transboundary movement of PPR in West Africa using phylogenetic analyses based on partial viral gene sequences. We collected samples and obtained partial nucleoprotein gene sequence from PPR-infected small ruminants across countries within West Africa. This new sequence data was combined with publically available data from the region to perform phylogenetic analyses. A total of fifty-five sequences were obtained in a region still poorly sampled. Phylogenetic analyses showed that the majority of virus sequences obtained in this study were placed within genetic clusters regrouping samples from multiple West African countries. Some of these clusters contained samples from countries sharing borders. In other cases, clusters grouped samples from very distant countries. Our results suggest extensive and recurrent transboundary movements of PPR within West Africa, supporting the need for a regional coordinated strategy for PPR surveillance and control in the region. Simple phylogenetic analyses based on readily available data can provide information on PPR transboundary dynamics and, therefore, could contribute to improve control strategies. On-going and future projects dedicated to PPR should include extensive genetic characterization and phylogenetic analyses of circulating viral strains in their effort to support the campaign for global eradication of the disease.

Complete genome sequence of a lineage I peste des petits ruminants virus isolated in 1969 in west Africa.

We report the complete genome sequence of a lineage I peste des petits ruminants virus (E32/1969) isolated in a Senegalese laboratory in 1969. This is the earliest peste des petits ruminants virus of any lineage sequenced to date and only the second lineage I virus available in public databases.