TYPE Original Research PUBLISHED 22 September 2023 DOI 10.3389/fvets.2023.1174560 Examination of critical factors OPEN ACCESS influencing ruminant disease dynamics in the Black Sea Basin EDITED BY Fernanda Dorea, Food and Agriculture Organization of the United Nations (Headquarters), Italy REVIEWED BY Margarida Arede 1*, Daniel Beltrán-Alcrudo 2, Jeyhun Aliyev 3, Ravikanth Reddy Poonooru, Tengiz Chaligava 4, Ipek Keskin 5, Tigran Markosyan 6, University of Missouri, United States Giorgia Angeloni, Dmitry Morozov 7, Sarah Oste 8, Andrii Pavlenko 2, Mihai Ponea 9, Experimental Zooprophylactic Institute of the Venezie (IZSVe), Italy Nicolae Starciuc 10, Anna Zdravkova 11, Eran Raizman 2, Jordi Casal 1 Jean Perchet, and Alberto Allepuz 1 World Organisation for Animal Health, France *CORRESPONDENCE 1 Departament de Sanitat i Anatomia Animals, Facultat de Veterinària, Universitat Autònoma de Margarida Arede Barcelona, Barcelona, Spain, 2 Food and Agriculture Organization of the United Nations (FAO), Regional margarida.decastro@uab.cat Office for Europe and Central Asia, Budapest, Hungary, 3 Food Safety Agency of the Republic of Azerbaijan, Baku, Azerbaijan, 4 Veterinary Department, National Food Agency, Ministry of Environmental RECEIVED 26 February 2023 Protection and Agriculture of Georgia, Tbilisi, Georgia, 5 Veterinary Control Central Research Institute, ACCEPTED 30 August 2023 Ministry of Agriculture and Forestry, Ankara, Türkiye, 6 Scientific Centre for Risk Assessment and Analysis PUBLISHED 22 September 2023 in Food Safety Area, Ministry of Agriculture, Nubarashen, Yerevan, Armenia, 7 Vitebsk State Academy of Veterinary Medicine, Vitebsk, Belarus, 8 University Institute of Technology Nancy-Brabois, Lorraine CITATION University, Villers-lès-Nancy, France, 9 National Sanitary Veterinary and Food Safety Authority, Bucharest, Arede M, Beltrán-Alcrudo D, Aliyev J, Romania, 10 Faculty of Veterinary Medicine, State Agrarian University of Moldova, Chisinau, Moldova, Chaligava T, Keskin I, Markosyan T, Morozov D, 11 Bulgarian Agency for Food Safety, Sofia, Bulgaria Oste S, Pavlenko A, Ponea M, Starciuc N, Zdravkova A, Raizman E, Casal J and Allepuz A (2023) Examination of critical factors influencing ruminant disease dynamics in the Introduction: Ruminant production in the Black Sea basin (BSB) is critical for Black Sea Basin. national economies and the subsistence of rural populations. Yet, zoonoses and Front. Vet. Sci. 10:1174560. transboundary animal diseases (TADs) are limiting and threatening the sector. To doi: 10.3389/fvets.2023.1174560 gain a more comprehensive understanding, this study characterizes key aspects COPYRIGHT © 2023 Arede, Beltrán-Alcrudo, Aliyev, of the ruminant sector in nine countries of the BSB, including Armenia, Azerbaijan, Chaligava, Keskin, Markosyan, Morozov, Oste, Belarus, Bulgaria, Georgia, Moldova, Romania, Türkiye, and Ukraine. Pavlenko, Ponea, Starciuc, Zdravkova, Raizman, Casal and Allepuz. This is an open-access Methods: We selected six priority ruminant diseases (anthrax, brucellosis, Crimean article distributed under the terms of the Congo haemorrhagic fever (CCHF), foot-and-mouth disease (FMD), lumpy skin Creative Commons Attribution License (CC BY). disease (LSD), and peste des petits ruminants (PPR)) that are present or threaten to The use, distribution or reproduction in other forums is permitted, provided the original emerge in the region. Standardized questionnaires were completed by a network author(s) and the copyright owner(s) are of focal points and supplemented with external sources. We examined country credited and that the original publication in this and ruminant-specific data such as demographics, economic importance, and journal is cited, in accordance with accepted academic practice. No use, distribution or value chains in each country. For disease-specific data, we analysed the sanitary reproduction is permitted which does not status, management strategies, and temporal trends of the selected diseases. comply with these terms. Results and discussion: The shift from a centrally planned to a market economy, following the collapse of the Soviet Union, restructured the ruminant sector. This sector played a critical role in rural livelihoods within the BSB. Yet, it faced significant challenges such as the low sustainability of pastoralism, technological limitations, and unregistered farms. Additionally, ruminant health was hindered by informal animal trade as a result of economic factors, insufficient support for the development of formal trade, and socio-cultural drivers. In the Caucasus and Türkiye, where diseases were present, improvements to ruminant health were driven by access to trading opportunities. Conversely, European countries, mostly disease-free, prioritized preventing disease incursion to avoid a high economic burden. While international initiatives for disease management are underway in the BSB, there is still a need for more effective local resource allocation and international partnerships to strengthen veterinary health capacity, protect animal health and improve ruminant production. Frontiers in Veterinary Science 01 frontiersin.org Arede et al. 10.3389/fvets.2023.1174560 KEYWORDS Black Sea, surveillance and control, ruminants, transboundary animal diseases, zoonoses 1. Introduction Nevertheless, key aspects linked with the dynamics of these diseases in the region remain poorly understood. Knowledge gaps Livestock production is critical for the subsistence of rural include disease geographic coverage and prevalence, morbidity and populations as a source of food, income, transportation, hides, mortality rates, economic impact, and risk factors influencing their and fertilizers, contributing to 40% of the agricultural economy spread and persistence. These gaps arise from weaknesses in a country’s worldwide (1). However, in recent decades, there has been a surge veterinary management programmes, which can be associated with and spread of endemic and exotic diseases affecting livestock (2, lack of human resources (authorities, veterinarians and technicians) to 3), which significantly impact the sector and threaten public sustain them, inadequate government funding for agriculture or health and welfare (4). This surge has been intensified by several livestock sectors, limited surveillance coverage (26), insufficient factors, including the high increase in international trade of legislative action, and lack of support for implementing biosecurity animals and animal products (3), rise in intensive farming driven measures (27). As a result, disease reporting is delayed, incomplete or by higher market demands for animal protein and increasing biased, leading to ineffective responses to disease outbreaks (28, 29). middle-class purchasing power (5–7), changes in land use (8), These challenges are more pronounced in rural areas of lower to shifts in migration and tourism patterns (9), and the effects of middle-income countries, as the BSB, where social inequality persists. climate change (9). In these regions, livestock, particularly ruminants, are ubiquitous and TADs such as foot-and-mouth disease (FMD), lumpy skin disease critical for livelihoods, and animal diseases hinder food security and (LSD), and peste des petits ruminants (PPR), along with zoonoses, the sector’s development. particularly anthrax, brucellosis (Brucella abortus and Brucella This study characterizes ruminant production and its importance melitensis), and Crimean Congo haemorrhagic fever (CCHF) (Table 1) around the BSB and describes the disease status and management are diseases that are either threatening ruminants or emerging in the efforts (i.e., surveillance and control activities) for the selected Black Sea Basin (BSB). Ruminant production is the most important ruminant diseases (Table 1) in nine countries of the region (i.e., livestock subsector in most countries in the region, ensuring food Armenia, Azerbaijan, Belarus, Bulgaria, Georgia, Moldova, Romania, security for rural populations and contributing significantly to Türkiye, and Ukraine). It also explores the most relevant factors that national economies (16–25). may influence the incursion and spread of these diseases in the region. TABLE 1 Overview of the studied diseases. Disease Agent Main domestic Transmission Vaccine host (s) availability Contact with B. anthracis Anthrax (10) Bacillus anthracis All mammals Yes spores Bacterial Brucella abortus Cattle Brucella (11) Direct/indirect contact Yes Zoonoses Brucella melitensis Sheep and goats CCHF virus Cattle, sheep, and CCHF (12) Tick-borne No • g. Orthonairovirus goats • f. Nairoviridae FMD virus Cattle, sheep, goats, FMD (13) Direct/indirect contact Yes • g. Aphthovirus and swine • f. Picornaviridae Viral LSD virus LSD (14) Cattle Arthropod vector Yes TADs • g. Capripoxvirus • f. Poxviridae Small ruminant morbilivirus PPR (15) Sheep and goats Direct contact Yes • g. Morbillivirus • f. Paramixoviridae g.: genus, f.: family. Frontiers in Veterinary Science 02 frontiersin.org Arede et al. 10.3389/fvets.2023.1174560 2. Materials and methods FPs received the report template via email, filled it in with preliminary information, and iteratively and upon request, added The current paper is a component of the GCP/GLO/074/USA further detail, following a back-and-forth exchange of emails and project, which contributes to the broader “Global Framework for virtual meetings. Data collection was carried out by the FPs in the Progressive Control of Transboundary Animal Diseases collaboration with local peers, and all activities were coordinated with (GF-TADs)” initiative. This project targets nine countries located national authorities to request and obtain approval for data sharing. around the BSB, namely Armenia, Azerbaijan, Belarus, Bulgaria, Data collection took place between October 2020 and December 2021. Georgia, Moldova, Romania, Türkiye, and Ukraine. Herein, Descriptive information and quantitative data were obtained Armenia, Azerbaijan, and Georgia are referred to as “Caucasus,” and analysed from completed report templates. Then, data were when the statement is true for the three countries, and Türkiye is assessed, and specific topics were selected to examine in this paper. referred to as either “Thrace” or “Anatolia” when specific differences To complement data on these topics, information was sourced from apply to each of the regions. national reports and websites of the Food and Agriculture The primary focus of the project is on six diseases that are relevant Organization of the United Nations (FAO), the World Organisation for the region: anthrax, brucellosis, CCHF, FMD, LSD, and for Animal Health (WOAH), and the World Bank. To assess the PPR. Consequently, this study focused on domestic ruminants (cattle, economic importance of ruminant production for each country, sheep and goats), which are the animal species most impacted by these we sourced data for the gross production value (GPV) of the main diseases. These species are also interchangeably referred to as large domestic production species from FAOSTAT (30). To find the ruminants (LR) and small ruminants (SR). proportional contribution of ruminant GPV to each country, A report template was designed to collect information from each we divided GPV for cattle, sheep, and goats, by the total GPV for all of the participating countries (Supplementary material S1). This domestic species in 2020. Finally, ruminant distribution maps for document was developed by four authors of this paper (AA, DB-A, ruminant populations (31–33) were sourced from FAO-NSAL JC, and MA) as a semi-structured questionnaire. The selection of (FAO’s Livestock Information, Sector Analysis and Policy) branch. topics was based on the project’s objectives and aimed at addressing Quantitative data was managed, cleaned, harmonized, and knowledge gaps in the BSB about the ruminant sector and the impact ® collated in Microsoft Office Excel (2019), RStudio (34), and analysed of the selected diseases. The initial version of the document was ® and visualised in Quantum GIS (35) and RStudio (34). presented and shared with respondents from the nine participating countries during a virtual meeting. The final version of the report template accounted for edits and suggestions provided by 3. Results the participants. The report template was divided into two sections. The first Selected topics from the nine participating countries were section focused on the ruminant demographics, types of ruminant organized into two sections following the structure of the report production, national and international trade, livestock markets, template: (1) study region and ruminant-specific information, and (2) slaughterhouses, seasonal movements, and value chains. The disease-specific information. second section focused on the six targeted diseases, requesting information on disease status, recent outbreaks, surveillance and control activities, awareness campaigns, and research activities 3.1. Study region and ruminant-specific in place. information Moreover, each report template requested information in two formats: narrative answers (e.g., description of a system or production 3.1.1. Study region type) and quantitative data in a database format (e.g., Excel datasheet). The main political changes and affiliations from countries of the In some cases, quantitative data could complement descriptive study region between 1988 and 2021 are illustrated in Figure 1. information. To have high-quality figures, we requested the highest Supplementary material S2 summarizes data for human and ruminant level of detail (e.g., the number of smallholder farms at the smallest demographics, relevant economic indicators, and other characteristics of administrative level) and, when applicable, exact locations (e.g., ruminant production. In 2020, most countries were classified as upper- georeferenced locations of a livestock market). Further instructions middle-income economies, with the exceptions of Ukraine and Romania, prompted respondents to refer to additional documents like local which had a lower-middle-income economy and a high-income veterinary authority national reports and national publications (i.e., economy, respectively (36). The median GDP per capita of each region grey literature). in 2020 was $4,547 USD, ranging from $3,725 USD in Ukraine to One focal point (FP) of each participating country was appointed $12,896 USD in Romania. For livestock production indicators, Moldova by FAO to answer the report template and collect country-specific and Bulgaria had the lowest contribution to agricultural information. FPs were carefully selected based on previous GDP at 23%, while Belarus had the highest at 57% (30). The proportion collaborations, the quality of their work, their expertise in the of ruminant GPV (per total domestic production species) ranged between ruminant sector and selected diseases, and access to the data necessary 23% in Moldova to 92% in Belarus (30). Further details about this for further analyses. FPs were based in each respective country and indicator are supplied in Supplementary material S3. were working (or had recently worked) within relevant national institutions (e.g., veterinary services, food safety authorities, or 3.1.2. Ruminant demographics national laboratories), during data collection. All nine FPs are The ruminant distribution varied significantly throughout the co-authors of this paper. study region, both for LR and SR. LR heads ranged from 159,000 in Frontiers in Veterinary Science 03 frontiersin.org Arede et al. 10.3389/fvets.2023.1174560 FIGURE 1 Political affiliations from 1988 to 2021 for the studied countries. FIGURE 2 Distribution of large ruminants (LR) – cattle – and small ruminants (SR) – sheep and goats – in the study region. Source: GLW4 (Gridded Livestock of the World) data modified with countries’ data and adjusted for FAOSTAT 2020 (31–33). Moldova to 18 million in Türkiye, whereas SR heads were lowest in entire region, more than 75% of herds keeping sheep and goats Belarus (148,000) and highest in Türkiye (54 million). Figure 2 were smallholdings. illustrates the spatial distribution for LR and SR in the region and shows higher abundance of LR in Belarus, certain regions of Türkiye, 3.1.4. Animal identification and registration western Georgia, and Azerbaijan, and higher number of SR in parts systems of Türkiye (Thrace and southeast Anatolia), Romania, and Most countries in the BSB had established National Animal Azerbaijan. Additionally, the figures highlight lower LR populations Identification and Traceability Systems (NAITS). In contrast, the in Ukraine, Moldova, southern Romania, and northern Bulgaria, and Caucasus had NAITSs under development, but not yet fully lower SR populations in Belarus, Ukraine, Moldova, and implemented at the time of data collection. In Azerbaijan, this system northern Bulgaria. was being developed through a European Commission (EC) framework. It entered a regional pilot stage in late 2021 and began a 3.1.3. Production types country-wide phased implementation over 2022 (37). In Armenia, the Countries classified ruminant production types using distinct Centre of Agribusiness and Rural Development (CARD), with support terminology. To allow for comparisons, production types were from the Austrian Development Agency (ADA) (38, 39), developed grouped based on herd size and commercial purpose into and conducted a pilot of its NAITS in the cattle sector in January 2022. smallholder and commercial farms, as defined in Similarly, in Georgia, after a 5-year project supported by FAO and Supplementary material S6. In the Caucasus and Romania, over 90% financed by the ADA and the Swiss Agency for Development and of cattle farms were smallholdings, while Belarus had the highest Cooperation (SDC) (40), the system was launched nationwide in proportion of cattle production in commercial herds. Across the February 2022 (40). Frontiers in Veterinary Science 04 frontiersin.org Arede et al. 10.3389/fvets.2023.1174560 3.1.5. National trade of live ruminants and Türkiye set up Veterinary Surveillance Points (VSP) along Recordings of live animal movements were linked to the existence migration routes. These premises primarily focused on mass of a NAITS in each country. Therefore, most countries in the region vaccination campaigns in Azerbaijan, but also served as rest points recorded these movements within a national centralized database. for supplying feed and water, as sanitary checkpoints for health Each registration included information regarding the individual status control, and anti-parasitic application in Georgia and identification of the animal and the farm of origin, the destination Türkiye. The mingling of animals from various herds, regions or farm, and a veterinary health report issued by an official veterinarian. even neighbouring countries was common in seasonal pastures. Conversely, Georgia did not have a recording system for animal Consequently, these animals were vaccinated either before going to movements. In Armenia and Azerbaijan, movements between pasture or during migration in VSPs. Furthermore, movements to provinces were registered, but the record consisted solely of a paper- seasonal pastures were recorded in centralized systems for based veterinary health certificate. These records were issued by movement control in Bulgaria, Romania (41) and Türkiye; however, official veterinarians and archived in regional divisions. There were no these recordings, similarly to national movements, were not done centralised databases for recording live animal movements in these in the Caucasus. three countries. In Belarus, Moldova, and Ukraine, ruminants kept in Live animal movements were characterized by a seasonal pattern smallholdings or smaller private farms in rural settings grazed that is not detailed in this paper. Nevertheless, it is worth noting that seasonally in fields surrounding their holdings, in an these movements significantly surged during cultural-religious agropastoral manner. celebrations such as Novruz, Kurban Bayram, and Ramadan Bayram in Azerbaijan and Türkiye, in which animals are transported to cities 3.1.6. International trade of live ruminants to be ritually slaughtered. Similarly, Easter and St George’s Day in Partner trading countries with the BSB region are presented in Bulgaria and Romania were also preceded by an increase in live the last two columns of Supplementary material S2. International animal movement due to the traditional consumption of mutton. trade of live animals was done based on country partnerships, Furthermore, it is important to highlight that livestock trade was contingent on the trust in the exporting country’s animal health closely linked to animal density in each region, the demand for animal capacity and/or the sanitary status for the main contagious protein in densely populated areas, the location of slaughterhouses, zoonoses and TADs (at a specific time) (42). To guarantee disease and specific commercial partnerships with regions or countries. For freedom on entry into a country, imported live ruminants were example, in Georgia, ruminant trade primarily occurred from west to accompanied by a health certificate validated by a veterinarian of east due to the high exports to Azerbaijan. As for Bulgaria, the the exporting country’s competent authority. Particularly for the southern regions, where LR and SR production was more intense, also importation of live animals (and animal products) into the EU, the had an increased movement of ruminants. Moreover, in Türkiye, intra-EU trade, and EU exports of live animals, TRACES (Trade ruminants were moved from small to large provinces, and more Control and Expert System) (43), an EC online platform, facilitates specifically from east to west and north to south of the country. sanitary certification required for trade and centralizes trade information. Thus, Bulgaria and Romania along with other BSB 3.1.5.1. Livestock markets countries exporting live animals or animal products into the EU, The role of livestock markets in live ruminant trade varied across used this platform. the region. Azerbaijan and Türkiye run ten and 150 licensed live Similar to national live animal movements, international trade animal markets, respectively, which played a significant role in was influenced by cultural-religious events. Therefore, a surge in live ruminant trade. During Kurban Bayram in these two countries, animal imports preceded Kurban Bayram and Ramadan Bayram in markets worked exceptionally to sustain the surge in animal Azerbaijan and Türkiye, and Easter and St George’s Day in Bulgaria movements. In Armenia, Georgia, and Bulgaria, these facilities existed and Romania. but were not as relevant for animal trade. In Belarus, official markets for live ruminant trade were absent, instead occasional fairs and exhibitions were held at the district level and on a small scale. In the 3.2. Disease-specific information same country, ruminant trade for breeding purposes occurred through state breeding companies. In Ukraine, smallholders used live 3.2.1. Disease status, surveillance, and control animal markets for local ruminant trade. activities Figure 3 illustrates the country-level disease statuses for each 3.1.5.2. Seasonal movements selected disease. Countries self-classified their disease status as Pastoralism includes seasonal movements to pastures and can endemic, sporadic, or absent (definitions in Supplementary material S6). be sub-classified as nomadism, transhumance, or agropastoralism An Absent status was subclassified for brucellosis as “officially free” and (definitions provided in Supplementary material S6). These for FMD as “officially free with or without vaccination” when WOAH practices are key to the seasonal sourcing of graze and water for officially recognised these disease statuses. livestock and were common across the study region. In Bulgaria, In Supplementary material S4, a table summarizes key details for the Caucasus, Romania, and Türkiye, transhumant animals were the six studied diseases in each of the countries of the BSB. Moreover, moved to summer pastures, often found in mountainous areas, in temporal trends of disease outbreaks per country from 2010 to 2020 spring and summer, and to lowland pastures or stables in autumn are shown in Supplementary material S5. In this subsection of the and winter. Migrating months had slight variations yearly results, we review the disease status and management practices applied depending on weather and pasture conditions. Georgia, Azerbaijan, in the region. Frontiers in Veterinary Science 05 frontiersin.org Arede et al. 10.3389/fvets.2023.1174560 FIGURE 3 Status of target diseases in the study region. Brucellosis status refer to Brucella abortus and Brucella melitensis. 3.2.1.1. Anthrax comprised the application of acaricide sprays to ruminants, including Anthrax was endemic or sporadic in all countries. All countries during seasonal migrations from early spring to late autumn, and implemented passive surveillance and, upon suspicion, applied further environmental tick elimination. Educational campaigns in Türkiye clinical examinations, sampling, and testing. Due to the environmental promoted contact restriction between livestock and wildlife, and tick nature of this disease, most national management programmes, in management. These campaigns were included in the state budget at addition to guidelines for disease containment and carcass disposal, no cost to farmers. For the remaining countries, CCHF had never also included regulations for historically infected fields (e.g., signalling, been reported in ruminants and there was no national surveillance fencing, digging restrictions, and awareness campaigns). Vaccination programme in place. At the time of data collection, no licensed was compulsory for all ruminants in Azerbaijan, and Moldova, and all vaccine was available for CCHF in ruminants. LR in Armenia. A risk-based vaccination approach was applied for all ruminants in Bulgaria, Georgia, Romania, Türkiye, and Ukraine, and 3.2.1.4. Foot-and-mouth disease exclusively for SR kept or moved to high-risk areas in Armenia. In The WOAH official FMD status varied between the two regions Belarus, anthrax vaccination was not conducted. of Türkiye: Anatolia was classified as endemic, and Thrace held FMD-free status with vaccination. FMD was sporadic in Armenia, 3.2.1.2. Brucellosis absent in Georgia and Azerbaijan, while in all other countries, Brucellosis was endemic in the Caucasus and Türkiye, sporadic in WOAH recognised the official status FMD-free without vaccination. Bulgaria, and absent in all other countries of the BSB. In 2012, Belarus FMD surveillance was active in the Caucasus and Türkiye, as well was officially recognised by WOAH as brucellosis-free, and to as in regions of Bulgaria and Romania. The countries of the Caucasus maintain this status, serosurveillance was conducted every three years. were collaborating with EuFMD through the Progressive Control Moreover, surveillance was exclusively passive for Georgia, and active Pathway for Foot and Mouth Disease (PCP-FMD) to design and and risk-based in all other countries. In most of the BSB, passive establish risk-based surveillance programmes. As part of these efforts, surveillance for brucellosis was associated with the report and they implemented NSP (Non-Structural Protein) and SP (Structural investigation of abortions in ruminants, which is a syndrome of this Protein) serosurveys to evaluate the FMD virus circulation, disease, but not exclusive to Brucella spp. infection. In Azerbaijan, seroconversion, and vaccination coverage. In regions bordering Georgia, and Türkiye, vaccination for brucellosis was mandatory for Thrace, Bulgaria conducted risk-based serosurveys on a sample of all ruminants and performed at the same time as serosurveillance. ruminants every three months. While in Romania, surveillance Brucellosis vaccination was not part of the national veterinary control focused on clinical examination of LR and SR on high-density plan in Belarus, Bulgaria, Moldova, Ukraine, or Romania. premises (e.g., live animal markets, exhibitions, ports, and airports), serosurveillance of all ruminants close to international borders, and 3.2.1.3. Crimean Congo haemorrhagic fever SR upon their arrival from seasonal pastures. CCHF was endemic in Georgia and Türkiye. These countries In Türkiye, the FMD management programme in 2021 aimed applied control measures upon outbreak identification, focusing on to achieve FMD-free status without vaccination in Thrace and tick control and community awareness campaigns. These activities FMD-free status with vaccination in Anatolia by 2025 (44). In Frontiers in Veterinary Science 06 frontiersin.org Arede et al. 10.3389/fvets.2023.1174560 Thrace, control measures comprised suspect FMD case culling, BSB. Furthermore, we explored key factors contributing to the restrictions on live animal imports from Anatolia, and strict introduction and spread of these diseases in the region. adherence to sanitary legislation. In Anatolia’s southeast provinces bordering FMD-endemic countries, surveillance activities were enhanced and risk-based. Moreover, in case of an FMD outbreak, 4.1. Post-Soviet Union reform Türkiye conducted a field investigation, and vaccination, established a cordon sanitaire, animal quarantine, and thorough The fall of the Soviet Union caused a deterioration of public cleaning and disinfection, organized training, and awareness infrastructures and services across the former Soviet Union (FSU) and campaigns, and closely monitored all premises within a 10 km Communist Bloc countries, significantly affecting agricultural and radius of the event. livestock sectors (18, 45–48). In BSB countries, except Belarus, FMD vaccination varied throughout the BSB. Türkiye vaccinated changes included the shift from collective and state-owned farms to LR twice a year, and SR once a year only in Thrace. In case of an private ownership, removal of government subsidies to the livestock outbreak in Anatolia, SR were also vaccinated in established sector (49), closure of large slaughterhouses (50), and depletion in protection and surveillance zones. In Azerbaijan, LR were vaccinated resource allocation to veterinary services (51). Such factors left twice a year (spring and autumn) and SR once a year, while Armenia, livestock production in the hands of unspecialized farmers, and applied the same strategy only in high-risk areas. Since 2017, Georgia unsupervised by veterinary services (52), resulting in increased has conducted vaccination exclusively in high-risk areas, based on disease incidence (52, 53). Thereafter, the region suffered a steep risk assessments, which considered seasonal migration, international decline in the number of ruminants (49, 54) and, in some countries, borders with FMD-endemic countries, live animal markets, and as Ukraine and Belarus, a significant abandonment of agricultural informal trade. lands (55). These abrupt structural changes were followed by a transition phase with gradual agricultural recovery and increasing 3.2.1.5. Lumpy skin disease productivity (56). Yet, rural poverty, particularly in the Caucasus and LSD was sporadic in Armenia, Azerbaijan, and Türkiye, and Moldova, persists and requires new and efficient policy measures that absent in all other countries. Surveillance activities varied: clinical enable technological development and access to market channels and examination was conducted in Belarus to a sample of LR in spring and services (51). EU’s farmer association model could aid smallholders summer, and in the six regions of Bulgaria bordering Thrace monthly. of the FSU to actively engage to improve their marketing, input Georgia had active participatory surveillance, Türkiye implemented supplies, and support services (57). both active and passive surveillance activities, and all other countries only applied passive surveillance. Compulsory vaccination was practised nationwide in Azerbaijan, Bulgaria, and Türkiye, and in 4.2. Rural livelihoods and pastoralism high-risk areas of Armenia and Georgia. Vaccination was not applied in Belarus, Moldova, Romania, or Ukraine. Pastoralism played a critical role in rural areas in most countries of the BSB (16–18, 20–25, 46, 58–60), creating a unique 3.2.1.6. Peste des petits ruminants interdependence between ruminants, farmers, and the environment PPR was endemic in Türkiye and absent in all other countries. In (61, 62). Preserving this practice is crucial, given its resilience to severe March 2021, Thrace was granted the classification of “PPR-protected climates in arid and inhospitable areas, socio-cultural importance, and area.” PPR surveillance varied across the BSB: Belarus did not conduct the potential opportunities brought to younger generations (62). it, Moldova, Ukraine, and Anatolia exclusively applied passive However, its sustainability in the BSB is a matter of concern. Ageing surveillance, while Thrace and all other countries applied active rural farmers show reluctance to adopt new technologies and surveillance. In Bulgaria, areas previously affected by PPR (2018 measures to improve animal production and health, and the mass outbreak) implemented enhanced surveillance, and regions bordering migration of younger populations to urban centres leaves families Thrace applied risk-based serosurveillance on a sample of SR every without essential support for farming activities (57). Moreover, they two months. In Romania, active surveillance included clinical have limited access to veterinary services also caused by ageing rural inspection of a sample of SR herds before and after pasture season. veterinarians, and difficulties in attracting young graduates due to Vaccination was implemented in Georgia, following the first PPR low-income prospects and prevailing urban migration trends (57). occurrence in 2016. In Türkiye vaccination was conducted, yet it These factors result in underperforming veterinary services (63) and ceased in Thrace after the region was granted a “PPR-protected area” high costs for disease management impeding improvements, even classification in March 2021. This measure, coupled with strict live SR when advancements are made at higher levels (28). Solutions for these movement restrictions from Anatolia to Thrace, aimed at Thrace’s challenges need to be explored, as building private veterinary capacity application for WOAH PPR zonal freedom status in 2023. In Anatolia, and developing training programmes for veterinary paraprofessionals. PPR vaccines were applied to all newborn SR and unvaccinated adults. In addition, initiatives addressing pastoralism’s limited sustainability and its associated risks to ruminant health and welfare are underway (64, 65). In Georgia (62), Türkiye, and Azerbaijan, VSPs 4. Discussion were established along migration routes. In Armenia, the “Project Coordination Platform for Sustainable Management of Natural In this paper, we summarized the ruminant production sector and Grazing Lands – Pastures and Grasslands” was launched to address reviewed the sanitary status and management of six diseases affecting pasture management-related problems in the country (66). ruminants (anthrax, brucellosis, CCHF, FMD, LSD, and PPR) in the Internationally, the Pastoralist Knowledge Hub (PKH) by FAO aids Frontiers in Veterinary Science 07 frontiersin.org Arede et al. 10.3389/fvets.2023.1174560 the development of synergies for dialogue and pastoralist development, initiatives involved significant investments to curb disease while an extension of the Performance of Veterinary Services (PVS) introduction and spread into Europe, while also promoting trade (67) evaluation tool prioritizes finding solutions to control animal opportunities (80, 81). Therefore, FMD and PPR statuses varied diseases in pastoralist areas (63). Collectively, these initiatives aim to between Thrace and Anatolia, leading to distinct classifications by foster and protect pastoralism while ensuring its sustainability. WOAH, along with distinct approaches for disease management and movement control in these two regions. 4.3. Disease management and related factors 4.4. The exception of CCHF Disease management in the Caucasus and Türkiye was often Türkiye and Georgia were the only countries in the BSB reporting inefficient. Nonetheless, improvements were being made in the field. the presence of CCHF in ruminants. In spite of this, past studies Particularly in the Caucasus, the full operability of the NAITSs is identified CCHF virological or serological evidence and the presence expected to make disease management programmes (68) and disease of competent vectors in most countries of the study region, except for traceability (69) more efficient. As a result, these improvements will Belarus (12, 82–84), while CCHF human cases were also notified in positively influence animal health and ruminant production, Bulgaria and Türkiye (84). Non-reporting of CCHF in ruminants was ultimately, leading to better trade opportunities and economic growth linked to two factors. Firstly, its exclusion from national veterinary in these countries. programmes resulted in the absence of routine official surveys, and Sociocultural-religious events in Türkiye and Azerbaijan secondly, the subclinical nature of the disease in these species allows prompted the implementation of contingency plans and extraordinary it to circulate unnoticed (85–87). Nevertheless, domestic ruminants measures, which, at times, proved inefficient in preventing disease play an important role in the epidemiology of the disease as they are introduction and spread. In fact, the epidemiological investigation involved in its vector life cycle (83) and amplification and spread of conducted upon the PPR incursion to Bulgaria in July 2018 concluded the virus (88, 89). Moreover, ruminant CCHFV antibody titers that the high demand and resulting price difference of mutton between correlate with virus presence in a region (84), as well as human Bulgaria and Thrace during these festivals contributed to increased disease incidence (82). Given CCHF’s public health threat, including informal movements of people and animals (70). potential human incurred deaths, the prudent course of action is to In the BSB, only Türkiye reported the presence of all studied include the disease in national veterinary programmes. This would diseases. This can be attributed to its unique conditions, including a ensure regular disease monitoring and prompt response to any large ruminant population, vast geographical area with socio- reported cases. economic disparities, and extensive rural regions. Moreover, its shared borders with six countries including Syria and Iraq, where social unrest leads to informal movement of people with their livestock, 4.5. Current initiatives create a significant pathway for disease spread (71, 72). Recognising the high risk to animal and public health through this route, Türkiye Achieving effective disease management requires not only efficient introduced legislative acts for border control and supervision of the resource allocation for national disease preparedness and response but main roads (73, 74). These acts are open to amendment, and they aim also promoting collaborations with other countries and unions. An to manage and identify informal/illegal trade for livestock and initiative that strengthens regional alliances for TADs management is products of animal origin, along with enforcing animal culling. the GF-TADs, a joint FAO and WOAH effort, created to support Following the implementation of these controls, a national report capacity building and the establishment of disease management highlighted a significant reduction of nearly 95% and 50% of programmes based on regional priorities (77). GF-TADs’ priority confiscated smuggled animals and animal products, respectively, diseases in the BSB include brucellosis, FMD, LSD, and PPR. Under caught during border controls conducted in 2011 and 2018. This this initiative, the Global Strategy for the Control and Eradication of demonstrates the successful impact of these actions (75). PPR aims to control and eradicate PPR and strengthen veterinary EU countries, such as Bulgaria and Romania, had high resource services (90, 91). Additionally, FAO’s PCP-FMD guides endemic allocation for disease management and prioritised the prevention of countries in progressively managing FMD risks and reducing its disease incursion to reduce economic losses. These countries followed impacts and viral circulation (92–94). harmonized live animal trade regulations set by the EC, enforcing additional control measures and trade restrictions (76) in the event of an exotic disease incursion. Therefore, responses to Bulgaria’s FMD 4.6. Limitations (2011), LSD (2016), and PPR (2018) outbreaks were quick and intensive (77). And LSD and FMD outbreaks resulted in an economic Study limitations were linked to country-specific factors and data burden estimated at €8 million (78), and $1.5 billion USD annually quality issues. Absent or not fully operable NAITSs are likely to have (79), respectively. To prevent disease re-emergence and further affected data validity, and completeness is limited due to unregistered economic losses, disease management activities established upon herds along with underreporting across the BSB. Underreporting is these events, were still in place as of 2021. often linked to farmers’ poor disease awareness, distrust in Moreover, Thrace’s proximity to Europe and shared borders with governmental authorities, risk of penalty or stigmatization, or at a the EU through Bulgaria and Greece, prompted the establishment of higher level, lack of capacity to enforce regulations (95) and low partnership programmes between the EU and Türkiye. These transparency. Additionally, variability in data availability and spatial Frontiers in Veterinary Science 08 frontiersin.org Arede et al. 10.3389/fvets.2023.1174560 resolutions between countries led to reduced accuracy of certain more effective disease management strategies contributing to indicators or made it impossible to compare and examine others. alleviating and preventing future outbreak scenarios. These Finally, data quality might have been affected by resource reallocation considerations go hand in hand with providing incentives for rural during the COVID-19 pandemic, which partly coincided with the development, by seeking financial aid, efficiently allocating financial two-year data collection period. and human resources, and most importantly ensuring the sustainability of the implemented strategies. 4.7. The armed conflict in Ukraine The armed conflict in Ukraine, starting in February 2022, had Data availability statement a significant impact on its livestock sector. Since its beginning, the conflict led to decreased agricultural production due to land The datasets presented in this article are not readily available for abandonment, animal losses from death or forced slaughtering, and public access due to restrictions imposed by the governmental entities reduced demand for meat and milk due to mass emigration (96). It of the nine participating countries. The data that support the findings has disrupted the accessibility to veterinary services, vaccines, of this study were used under license from these entities and are medication (97), and critical inputs, such as feed and fodder (96), subject to confidentiality and legal constraints. Requests to access the compromising disease prevention and control, and increasing the datasets should be directed to margarida.decastro@uab.cat. risk of stress, malnourishment, and susceptibility to disease in livestock. Moreover, amongst security issues, unavailability of consumables and equipment, and competing urgent priorities, Ethics statement appropriate carcase disposal became challenging. These effects are expected to reshape ruminant demographics, its associated Ethical review and approval was not required for the study of production sector, and value chains, particularly in front-line animals in accordance with the local legislation and regions. International cooperation is vital to address the institutional requirements. consequences on livestock health and revive the sector post- conflict. Guidelines aiming to support the livelihoods of livestock- keeping communities in humanitarian emergencies that affect Author contributions livestock are in place (98, 99), being used to alleviate the consequences of the presented conflict. AA, DB-A, JC, and MA developed the report template and contributed to the conception and design of the study. JA, TC, IK, TM, DM, AP, MP, NS, and AZ were hired as country FPs to fill in the report 5. Conclusion template and provide quantitative data and descriptive information for the project. SO wrote a document summarizing preliminary This study provides a comprehensive overview of the ruminant information. MA performed the data management, descriptive production sector and the management of six major diseases of analysis and visualization materials, and wrote the first draft of the concern in the BSB. By examining the effects of the post-soviet reform, manuscript. All authors contributed to the article and approved the the importance of pastoralism, differences in disease management and submitted version. countries’ response to disease incursion, as well as the influence of cultural events and political affiliations on live animal trade, we have gained a valuable understanding of how these different factors work Funding together to determine disease dynamics in the region. Unlike the other studied diseases, CCHF was not included in The project GCP/GLO/074/USA “Global Framework for the veterinary management plans, and not surveyed in ruminants Progressive Control of Transboundary Animal Diseases (GF-TADs)” across the region, presenting a public health threat. Furthermore, was funded by the United States Department of Defense, Defense the armed conflict in Ukraine starting after data collection will Threat Reduction Agency (DTRA). The content of the information likely have a significant impact on ruminant production and animal does not necessarily reflect the position or the policy of the Federal disease emergence in this country, with potential spread to Government of the United States, and no official endorsement should neighbouring countries. be inferred. Finally, despite recent developments in veterinary infrastructures, including the implementation of NAITSs in the Caucasus, substantial support from international agencies and Acknowledgments targeted initiatives for ruminant disease management, the need to improve animal health persists, particularly in rural and remote The authors acknowledge the national authorities from the nine regions. A thorough understanding of the primary challenges, countries for providing all the data and documents on ruminant needs, and constraints faced by smallholders in each specific demographics and diseases. We also acknowledge Giuseppina Cinardi country context is essential. Establishing priorities and closely from FAO-NSAL for her contribution in generating GLW 4 maps for assessing them in collaboration with farmers, national stakeholders, ruminants distribution. These maps, presented in Figure 2, were and international agencies, will aid in identifying opportunities for adjusted to incorporate data obtained during the project. Frontiers in Veterinary Science 09 frontiersin.org Arede et al. 10.3389/fvets.2023.1174560 Conflict of interest organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or The authors declare that the research was conducted in the claim that may be made by its manufacturer, is not guaranteed or absence of any commercial or financial relationships that could endorsed by the publisher. be construed as a potential conflict of interest. Supplementary material Publisher’s note The Supplementary material for this article can be found online All claims expressed in this article are solely those of the at: https://www.frontiersin.org/articles/10.3389/fvets.2023.1174560/ authors and do not necessarily represent those of their affiliated full#supplementary-material References 1. FAO. The state of food and agriculture. Livestock in the balance; (2009). Available 20. General Directorate of Agricultural Research and Policies. Turkey Country Report at: https://www.fao.org/3/a-i0680e.pdf on Farm Animal Genetic Resources. Food and Agriculture Organization. (2004). Available at: https://www.fao.org/3/a1250e/annexes/CountryReports/Turkey.pdf 2. Berezowski J, Lindberg A, Ward M. Surveillance against the odds: addressing the challenges of animal health surveillance. Prev Vet Med. (2015) 120:1–3. doi: 10.1016/J. 21. Sen O, Ruban S, Getya A, Nesterov Y. 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