key: cord-0936958-3qr4ihrf authors: Fanelli, Angela; Muñoz, Olga; Mantegazza, Luca; De Nardi, Marco; Capua, Ilaria title: Is the COVID‐19 pandemic impacting on the risk of African Swine Fever virus (ASFV) introduction into the United States? A short‐term assessment of the risk factors date: 2021-10-02 journal: Transbound Emerg Dis DOI: 10.1111/tbed.14330 sha: 26a20c7104d9df5a90ba2c2fa479a8e1af846fee doc_id: 936958 cord_uid: 3qr4ihrf African swine fever (ASF) is a contagious disease with high mortality in domestic and feral swine populations. Although it is not a zoonosis, its spread may have severe socio‐economic and public health consequences. The activities of veterinary services are essential for controlling ASF outbreaks within a country, but also for diminishing its threat of spread to neighbouring countries, and for recognizing its entry into countries that are currently free. ASF requires quick responses and permanent monitoring to identify outbreaks and prevent spread, and both aspects can be heavily undercut during the COVID‐19 pandemic. This paper analyses changing patterns of the main drivers and pathways for the potential introduction of ASFV into the United States during the COVID‐19 pandemic, including international movements of people, swine products and by‐products. Data on commercial flights and merchant ships was used as a proxy to indirectly assess the flow of illegal products coming from ASF affected countries. Results from this study highlight a decreasing trend in the legal imports of swine products and by‐products from ASF affected countries (Sen's slope = −99, 95% CI: −215.34 to −21.26, p‐value < 0.05), while no trend was detected for confiscations of illegal products at ports of entry. Additionally, increasing trends were detected for the monthly number of merchant ships coming from ASF affected countries (Sen's slope = 0.46, 95%CI 0.25–0.59), the monthly value of imported goods ($) through merchant ships (Sen's slope = 1513196160, 95%CI 1072731702–1908231855), and the monthly percentage of commercial flights (Sen's slope = 0.005, 95%CI 0.003–0.007), with the majority of them originating from China. Overall, the findings show an increased connection of the United States with ASF affected countries, highlighting the risk posed by ASF during a global public health crisis. African Swine Fever (ASF) is a contagious haemorrhagic viral disease of domestic and wild pigs, causing substantial economic losses to pig farming in the affected countries. It is one of the most important pig diseases due to the severe socioeconomic consequences for affected countries. For example, a study modelling the global impact of a major ASF outbreak in China, showed that this would cause an increase of pork prices by 17%-85% , along with other domino effects, such as increases in prices of other meats due to increased demand, decrease in feed prices, and decreased availability of animal source foods, which are fundamental for human health nutrition (Mason-D'Croz et al., 2020) . As such, ASF is one of the most important emerging infectious diseases in the swine industry, causing major veterinary, economic and food production concerns due to its continued outbreaks and global spread (Gaudreault et al., 2020) . Underlining its importance is the fact that it is a notifiable disease according to the World Organisation for Animal Health (OIE) (OIE, 2021a) . Specifically, ASF was listed in the ex-list A which included transmissible diseases that have the potential for very serious and rapid spread, irrespective of national borders, with a great impact on the international trade of animals and animal products (https://www. oie.int/en/what-we-do/animal-health-and-welfare/animal-diseases/ old-classification-of-diseases-notifiable-to-the-oie-list-a/). The epidemiology of ASF is complex with different epidemiological patterns of infection occurring in Africa, Europe and Asia due to the presence of wild hosts and vectors, environmental conditions, human behaviour and characteristics of the viruses circulating in the regions giving rise to a wide range of clinical forms (Gallardo et al., 2015) . Since there are no commercial vaccines currently available against ASFV (Sang et al., 2020) , control measures are limited to testing and mass slaughtering of infected and in-contact pigs. Also the implementation of high biosecurity standards are critical to protect swine populations, however, these are more likely to be applied in intensive rearing farms than in small and backyard production (Danzetta et al., 2020) . Laboratory diagnosis of ASF consists of detection of the virus and immune responses, using a variety of commercially available tests (Gallardo et al., 2019) , and guidelines for diagnosing and reporting have been developed by the OIE (OIE, 2019). At the time of revising the paper (March 2021), the disease is continuing to spread across Asia and Eastern Europe at a worrying rate, with millions of pigs being culled to halt its spread (Table S1 ). In addition to animal health concern, the disease has a large impact on international exports of pig products and on producer prices in the domestic markets (Niemi, 2020) . The impact is highest in countries with a significant commercial pig industry. The United States is the world third-largest producer of pork and pork products (12,843 tons of pork produced in 2020), thus the entrance and spread of ASFV would have a huge socio-economic effect. In 2020, the value of U.S. pork exports to the world increased by 11% from the prior year, with China, Japan and Mexico being the top trade partners. The reason of the U.S. export growth is mainly driven by the strong global demand for pork product due to decreased Chinese production resulting from ASF (USDA, 2021a). The United States has never had a case of ASF and there are strict import requirements to prevent any form of ASF to enter into the country. Figure S2 ). Timely and accurate reporting allows to prevent F I G U R E 1 Summary of the components that should be considered to evaluate changing patterns of the main drivers and pathways for the potential introduction of ASFV into the United States during the COVID-19 pandemic. The key points hit by the COVID-19 are presented in red. the entry of ASFV from affected areas. Thus, the lack of knowledge of animal health status in certain areas could have heightened the risk of ASFV entry through swine products/by-products legally imported. Conversely, the risk of entry is expected to be reduced when considering that the COVID-19 pandemic has negatively affected the world meat trade with a global decline of meat imports and a decrease of meat prices (FAO, 2020b) . Similarly, the risk of ASFV entry through smuggling of pork in passengers' luggage could have decreased due to the reduction of the number of people travelling. However, the number of import/export inspectors has fallen worldwide (OECD, 2020), thus the border controls could have been compromised. Considering all the above, this study aims to investigate changing patterns of the main drivers and pathways for the potential introduction of ASFV in the United States during the COVID-19 pandemic. Figure 1 shows the main drivers and pathways for the potential introduction of ASF into the United States through the legal and illegal imports of swine products and by-products. For the illegal importation, the number of international flights, ships and passengers from ASF affected countries are relevant indicators as they are assumed to influence the risk of illegal import. Considering that ASF control measures are required both before departure and on arrival to effectively prevent the disease transmission across borders, the main stakeholders influencing the risk of ASF entry into the United States are identified as following (depending on the different national institutional structure additional stakeholders, not listed here, may be relevant too): • National Veterinary Services (VS) (governmental bodies/laboratories) of ASF affected trade partners and countries from which illegal products originate: personnel involved in animal disease monitoring and surveillance activities responsible to prevent the export of ASFV infected products. Overview of the data required Flow of swine products/by-products legally imported from ASF affected countries Data on imported swine products and by-products was obtained from the USDA Global Agricultural Trade System (GATS) (USDA, 2021b). GATS database contained the quantities (MT 6 /pieces) and value ($) of imported products by month and country of origin. Considering that the risk for swine products and by-products to be infected/contaminated and maintained infectious ASFV depends on the type of matrix (EFSA AHAW Panel, 2014), we divided data in four main categories: frozen, fresh or chilled, processed and raw hides and skins (not pre-tanned). Fully tanned and processed hides and skins were not included, as not representing a risk (Ministry of Agriculture and Forestry, 2008). Since the unit of measure of raw hides and skins (pieces) differs from the other products (MT), they were not included in the quantitative analysis. The information on ASF affected trade partners was used to build six time series: (i) monthly number of ASF affected trade partners, (ii) monthly quantity of swine products and byproducts imported from ASF affected countries, (iii) monthly percentage of swine products and by-products imported from ASF affected countries over the total quantity of swine products imported, (iv) monthly quantity of fresh or chilled swine products and by-products imported from ASF affected countries, (v) monthly quantity of frozen swine products and by-products imported from ASF affected countries, and (vi) monthly quantity of processed swine products and by-products imported from ASF affected countries. Flow of illegal swine products/by-products from ASF affected countries The flow of illegal swine products/ by-products from ASF affected countries was assessed using: (i) data on illegally imported domestic swine products and by-products confiscated in the United States ports of entry obtained from the Agricultural Quarantine Activity Work Accomplishment (WADS), (ii) data on wild suids products confiscations obtained from the Law Enforcement Management Information System (LEMIS) database. Access to these databases was provided by the CBP and FWS personnel, respectively. As data retrieved from WADS was not homogeneous (e.g., some records described the products in kilograms other as number of confiscated packages), the target of the analysis was the "event" intended as the record of a single confiscation. The information was used to build three time series: (i) monthly number of ASF affected countries of origin, (ii) monthly number of events from ASF affected countries recorded by CBP, (iii) monthly percentage of events from ASF affected countries over the total number of events recorded by CBP. Additionally, the following relevant indicators imports of goods ($) from ASF affected countries over the total imports. The Sen's method was used to determine whether there was a positive or negative trend in the time-series with a significance level alpha set at 0.05 (Sen, 1968) . This method computes linear trend in timeseries, which can be presented as an upwards/positive or a downwards/negative trend. It has many advantages (e.g., data does not need to conform to any particular distribution) that have made it very useful in time series analysis in different fields (Fanelli, Perrone et al., 2021; Fanelli, Tizzani et al., 2021; Marques da Silva et al., 2015) . All the time series were formatted into a time-series object using the ts () function in the R software 3.5.2 (R Core Team, 2018). Out of 15 time-series analyses performed only 6 were significant and are presented in Table 1 Details are provided in Sections 3.1.1. and 3.1.2. Seven trade partners (28.57%) were identified as ASF affected. These were China, Germany, Hungary, Lithuania, India and Poland (further details in Figure S3 and Table S2 ). In this study Italy was considered as free of ASF, although the disease is endemic in Sardinia Island (Franzoni et al., 2020) . The situation of Sardinia differs from that in other territories due to the long lasting endemicity of the disease since 1978, thus the EU banned swine export from Sardinia (Decision 2014/709/EU) and a strict control is applied to the animal products movement from the Island. The total imports of swine products from ASF affected countries was 98960 MT, corresponding to 11.22% of the total imports during the study period. Details on the monthly number of ASF affected trade partners and the quantity of swine products and by-products imported are shown in Figure 2 . F I G U R E 2 Monthly U.S. imports between January 2019 and February 2021: (a) number of ASF affected trade partners, (b) quantity of swine products and by-products imported from ASF affected countries, (c) percentage of swine products and by-products imported from ASF affected countries over the total quantity of swine products imported. Please note that raw hides and skins are not included in the charts. were (34.5%) ASF affected 7 (Table S3) which accounted for 316 confiscations (37.6%). Table 2 shows the number of events per ASF affected countries of origin. China represents the ASF affected country from which the majority (71%) of the illegal products originate. Table S4 ). A peak of confiscations was detected in September 2020, when 92 events from ASF affected countries occurred. Out of these, 90 were records of swine products and byproducts from China. Considering the confiscation of illegally imported wild suids products retrieved from the LEMIS database, there are only 10 records originating from seven different countries. Among these, three products were from ASF affected countries. These include two trophies of warthog from Zambia and tusks of a wild suid from Cambodia. The monthly data on U.S. commercial flights between January 2019 and February 2021 are described in Figure 5 . The analysis of air transportation from ASF affected countries showed no significant trend using the Sens' method considering the number of passengers transported (Table S6 ) and the number of departures performed by international commercial flights (p-value > 0.05, Table S8S ). When normalized with the total number of departures, the monthly percentage of departures from ASF affected countries noted a slightly significant increase (Sen's slope = 0.005, 95%CI 0.003-0.007), with a peak in May 2020 when 25% of the flights performed to the U.S. originated from ASF affected countries (Figure 5d ). In this month, most of the commercial Poland 9 Togo 1 Vietnam 5 Monthly U.S. data on illegal swine products and by products between January 2019 and February 2021: (a) number of ASF affected countries of origin, (b) number of events from ASF affected countries recorded by CBP, (c) percentage of events from ASF affected countries over the total number of events recorded by CBP. flights from ASF affected countries came from China (43%), followed by South Korea (33%) ( Table S7 ). The U.S. international routes of merchant ships included 24% (56/234) of ASF affected countries (Table S9) If done in compliance with the official regulation (e.g., appropriate heat treatment, controls in place etc) the risk of ASFV introduction through the legal importation of swine products and by-products from ASF affected countries is considered to be low. It is worth mentioning that the analysis performed not only reveals a downtrend in the total amount of swine products and by-products imported, but also a decreasing import of frozen products from ASF affected countries. This is important because the risk for different matrices to maintain infectious ASFV at the moment of transportation varies from very high for frozen meat to negligible for meat cooked for 70 • C for 30 min (EFSA AHAW Panel, 2014). The ASF affected U.S. trade partners identified in this study reported the implementation of zoning to control ASF, and China declares to apply also the compartmentalization (OIE, 2021, Table S5 ). The zoning principle consists in defining a geographic area to contain ASF outbreaks. The areas outside of these control zones are diseasefree zones. This implies that all pork production businesses within the disease free-zones must operate at a high biosecurity standard, and do not have parts of their business outside the disease-free zone (OIE, 2018) . Conversely, compartmentalisation consists in a single or multiple connected facilities dealing with pig populations free of ASF whereas ASF is assumed to be present in the rest of the country. Compartments adopt high biosecurity standards required to control ASFV, thus they are mostly implemented by single companies that have integrated production processes (Cowled et al., 2019) . ASF control measures reported by the countries to the OIE are accessible through the OIE-WHAIS database. The information is available till 2019/2020 but data is missing for some periods due to delays in reporting (e.g. India). Some U.S. trade partners (e.g., Poland) had difficulties in timely reporting ASF outbreaks during 2020 (Supplementary material: Figure 1S ). This delay may be due to various intrinsic and extrinsic factors, including the COVID-19 emergency. The COVID-19 related disruption of the functioning of the national veterinary services, like many other services, is plausible (FAO, 2020a; Gortázar & de la Fuente, 2020). The activities of veterinary services are essential for early detection and controlling ASF outbreaks within a country, and consequently to reduce the risk of further spread to neighbouring countries. Although it is only a hypothesis, we suggest that the COVID-19 pandemic has severely affected the control and surveillance of animal diseases. ASF requires quick responses and permanent monitoring to identify outbreaks and prevent spread, and both aspects could have been heavily undercut during the COVID-19 pandemic. It is believed that the illegal importation of swine products and by-products from ASF affected countries represents the main source of ASFV introduction into free areas. Several risk assessments have been performed focusing on the flow of smuggled swine products from ASF affected countries Sugiura, Lei et al., 2020; Wooldridge et al., 2006) . During the COVID-19 pandemic, a dramatic decline in the ASF entry risk into Japan through this route was reported, and attributed to a decrease in the number of air travellers from China (Sugiura, Kure et al., 2020) . In this study, no changing trend was detected in the monthly confiscations of swine products from ASF affected countries at the U.S. port of entries. However, a peak of con- Only a small percentage of illegally imported products is generally detected at the ports of entry, as a results of a limited inspection workforce and budgetary restrictions over time (Brown & Bevins, 2018 Specifically, it led to a reduction in the amount of passenger flights and belly cargo, requiring an increase in the number of flights that carry cargo only (Bartle et al., 2021) . However, determining the impact of the COVID-19 crisis on the air freight transport is complex, considering that the capacity demanded for some goods has increased, while the demand for others has lapsed. In this study, only the departures performed and passengers from ASF affected countries were evaluated. This should be considered when interpreting the results presented. A high percentage of trade routes from ASF affected countries was also detected. This is not surprising as goods are generally produced in regions where the cost of labour is low (e.g., Asia). In line with the commercial air transportation, increased trends in the number of ASF affected countries of origin of merchant ships and goods (in value-$) transported were also observed during the COVID-19 pandemic. This is of relevance as the waste disposal from international ships has historically been one of the most important ways for ASFV introduction into free areas (Mur et al., 2012) . No information was available for the movements of passengers and number of merchant ships, but it was considered the dollar value of the goods imported. This provides a realistic information of the changes in volume between years, assuming that the type of goods imported from each country per each port is more or less homogeneous in time. Additionally, this study is based on two consecutive years, with limited variation of dollar inflation (Table S10) . Under these assumptions, the increasing trend seems to be due to a real increase in imports rather than a price increase. It is important to consider that the increased number of trade partners that are ASF affected is also due to the fact that some countries already trading with the United States became ASF countries during the study period (e.g., India). should be focused on the U.S. border control measures and should be administered to experts from U.S. governmental bodies. Specifically, the questions should consider: (i) capacity to work on animal health activities at farm level (difficulties to maintain good biosecurity, movement restrictions limit farmers' capacity to reach out to their veterinarian), (ii) disease surveillance activities (outbreak investigation and disease reporting disrupted due to logistical issues), (iii) laboratory diagnostics (shortages of lab reagents and reduced intensity of lab testing for animal diseases ), (iv) control of imported foods (sampling and analysis of food), (v) reallocation of veterinary staff to national COVID-19 emergency response teams. In conclusion, this study highlights an increased connection of the U.S. with ASF affected countries during COVID-19 pandemic. The findings presented did not aim to provide an estimate of the risk of introduction of ASFV in the United States. but they point out important aspects to be considered when performing a risk assessment during a global public health emergency. The long-term consequences of this pandemic on countries capacities to control and prevent ASF are still unknown. Nonetheless, it remains fundamental to ensure that the ASF risk is not underestimated. In this sense, a risk assessment that includes EKE and covers all the aspects influencing the ASFV risk of introduction into the United States is necessary to inform polic makers and international agencies on the risk posed by ASF during a public health emergency status. Lastly, the circulation of ASFV in the Dominican Republic represents a great risk for the whole Americas Region. The disease is likely to further spread in the highly interconnected Caribbean Islands, given the socio-cultural context of this area, the important movements of ships, flights, and population of emigrants from Dominican Republic. Therefore, an increased surveillance effort at borders of every American country is needed to assure early detection of ASFV and rapid reaction. The authors declare that there is no conflict of interest. Ethics approval was not required for this study. The data that supports the findings of this study are available in the supplementary material of this article. This research was supported by the Circular Health Fellowship program of the One Health Center of Excellence of UF. Open Access Funding provided by Universita degli Studi di Bari Aldo Moro within the CRUI-CARE Agreement. Angela Fanelli https://orcid.org/0000-0002-8204-1230 Olga Muñoz https://orcid.org/0000-0002-1431-1761 Sustainability and air freight transportation: Lessons from the global pandemic A review of African swine fever and the potential for introduction into the United States and the possibility of subsequent establishment in feral swine and native ticks Technical White Paper: Business Continuity in the Face of African Swine Fever: Compartmentalisation and Company Biosecurity Ausvet and One Health Scientific Solutions >November ABCD African swine fever: Lessons to learn from past eradication experiences. A systematic review Scientific opinion on African swine fever Spatial and temporal dynamics of wild boars Sus scrofa hunted in Alpine environment Crimean-Congo Hemorrhagic Fever (CCHF) in animals: global characterization and evolution from Guidelines to mitigate the impact of the COVID-19 pandemic on livestock production and animal health African swine fever circulation among free-ranging pigs in sardinia: Data from the eradication program. Vaccines, 8, 549 African swine fever (ASF) diagnosis, an essential tool in the epidemiological investigation Assessment of African swine fever diagnostic techniques as a response to the epidemic outbreaks in eastern european union countries: How to improve surveillance and control programs African swine fever virus: An emerging DNA arbovirus Quantitative approach for the risk assessment of African swine fever and Classical swine fever introduction into the United States through legal imports of pigs and swine products Risk of African swine fever virus introduction into the United States through smuggling of pork in air passenger luggage Could African swine fever and classical swine fever viruses enter into the United States via swine products carried in air passengers' luggage? Transboundary and Emerging Diseases Bulletin de l'OIE, Border control measures to prevent introduction of ASF. Lessons from the Japanese experience World Organisation for Animal Health Rainfall and river flow trends using Mann-Kendall and Sen's slope estimator statistical tests in the Cobres River basin Modelling the global economic consequences of a major African swine fever outbreak in China Import risk analysis: Hides and skins from specified animals. Ministry of Agriculture and Forestry Risk of African swine fever introduction into the European Union through transportassociated routes: returning trucks and waste from international ships and planes Impacts of African swine fever on pigmeat markets in Europe NPPC Heralds Signing Of AG inspectors bill -National pork producers council PVS Evaluation Follow-Up mission report-Brazil African swine fever (infection with African swine fever virus) (pp. 1-18). Terrestrial Animal Health Code African swine fever World Animal Health Information System Covid-19 in Latin America A language and environment for statistical computing. R foundation for statistical computing Progress toward development of effective and safe African swine fever virus vaccines Estimates of the regression coefficient based on Kendall's Tau Change in the ASF entry risk into Japan as a result of the COVID-19 pandemic. Transboundary and Emerging Diseases Assessing the risk of ASFV entry into Japan through pork products illegally brought in by air passengers from China and fed to pigs in Japan USA Trade Online POSTAL SERVICE: Volume, performance, and financial changes since the onset of the COVID-19 pandemic United States Department of Transportation COVID-19 and e-commerce a global review Global agricultural trade system (GATS) Qualitative Assessment of the likelihood of African swine fever virus entry to the United States: Entry Assessment NPPC remains focused on ASF prevention efforts Quantitative risk assessment case study: Smuggled meats as disease vectors Is the COVID-19 pandemic impacting on the risk of African Swine Fever virus (ASFV) introduction into the United States? A short-term assessment of the risk factors Marco De Nardi https://orcid.org/0000-0001-5648-257X Ilaria Capua https://orcid.org/0000-0002-7072-2581 ENDNOTES 1 https://www.ecfr.gov/cgi-bin/text-idx?SID=9babc721e6ebd9cdc085 a3396f1c97ce&mc=true&tpl=/ecfrbrowse/Title09/9cfr94_main_02.tpl 2 https://www.aphis.usda.gov/aphis/ourfocus/animalhealth/ animal-and-animal-product-import-information/ animal-health-status-of-regions 3 https://eur-lex.europa.eu/legal-content/EN/TXT/HTML/?uri=OJ:L:2021: 129:TOC 4 https://uscode.house.gov/view.xhtml?path=/prelim@title21/ chapter12&edition=prelim 5 https://www.govinfo.gov/content/pkg/CFR-2012-title9-vol2/pdf/ CFR-2012-title9-vol2-part327.pdf 6 MT: Metric Tons 7 The number of events from ASF affected countries was computed considering the ASF first occurrence reported by the countries to the OIE. For instance, the first occurrence of ASF in Germany is on 09/09/2020. Illegal products from Germany confiscated by CBP before September 2020 were not considered.