key: cord-0957922-vt20fie0 authors: Adlhoch, Cornelia; Fusaro, Alice; Kuiken, Thijs; Niqueux, Eric; Staubach, Christoph; Terregino, Calogero; Guajardo, Irene Muñoz; Baldinelli, Francesca title: Avian influenza overview February – May 2020 date: 2020-06-30 journal: EFSA J DOI: 10.2903/j.efsa.2020.6194 sha: 1bdc30da8a6e174dbf8154e3b3f867bec9d21f9c doc_id: 957922 cord_uid: vt20fie0 Between 16 February and 15 May 2020, 290highly pathogenic avian influenza (HPAI) A(H5) virus outbreakswere reported in Europe in poultry (n=287), captive birds (n=2) and wild birds (n=1)in Bulgaria, Czechia,Germany,Hungary andPolandand two low pathogenic avian influenza (LPAI) A(H7N1) virus outbreaks were reported in poultry in Italy. 258 of 287 poultry outbreaks detected in Europe were secondary outbreaks, suggesting that in the large majoryty of cases the spread of the virus was not due to wild birds.Allthe HPAI outbreaks were A(H5N8) apart from three,which were reported as A(H5N2) from Bulgaria. Genetic analysis of the HPAI A(H5N8) viruses isolated from the eastern and central European countries indicates that this is a reassortant between HPAI A(H5N8) viruses from Africa and LPAI viruses from Eurasia. Two distict subtypes were identified in Bulgaria, a novel reassortant A(H5N2) and A(H5N8) that is persisting in the country since 2016. There could be several reasons why only very few HPAI cases were detected in wild birds in this 2019‐2020 epidemic season and a better knowledge of wild bird movements and virus‐host interaction (e.g. susceptibility of the hosts to this virus) could help to understand the reasons for poor detection of HPAI infected wild birds. In comparison with the last reporting period, a decreasing number of HPAI A(H5)‐affected countries and outbreaks were reported from outside Europe. However, there is considerable uncertainty regarding the current epidemiological situation in many countries out of Europe. Four human cases due to A(H9N2) virus infection were reported during the reporting period from China. This scientific report provides an overview of highly pathogenic avian influenza (HPAI) virus outbreaks detected in poultry, captive and wild birds and noteworthy outbreaks of low pathogenic avian influenza (LPAI) virus in poultry and captive birds, as well as human cases due to avian influenza (AI) virus, reported in and outside Europe between 16 February and 15 May 2020. The background, terms of reference and their interpretation are described in Appendix A and the data and methodologies are reported in Appendix B. Avian influenza outbreaks in European countries and in other countries of interest between 16 February and 15 May 2020 2.1. • No human infections with HPAI or LPAI viruses of the same genetic composition as those currently detected in domestic and wild birds in Europe have been reported from the EU/EEA Member States. • Four infections of children with A(H9N2) virus have been reported from China. • Since 2005, Europe has experienced six HPAI A(H5) incursions and three of them occurred in the last four years (2016-2017, 2017-2018 and 2019-2020) . • In Europe, between 16 February and 15 May 2020 (based on the Animal Disease Notification System (ADNS)): -287 HPAI A(H5N8) outbreaks were reported: 263 in poultry in Hungary, 14 in poultry in Poland, 2 in poultry, 2 in captive birds and 1 in a wild bird in Germany, 4 in poultry in Bulgaria, 1 in poultry in Czechia; 3 HPAI A(H5N2) outbreaks were reported in poultry in Bulgaria; -two LPAI A(H7N1) outbreaks were reported in poultry in Italy. • The genomic characterisation of the HPAI A(H5) viruses detected in domestic and wild birds in Europe indicates the circulation of three genotypes of clade 2.3.4.4b. Specifically, a reassortant HPAI A(H5N8) between HPAI A(H5N8) viruses from Africa and LPAI viruses from Eurasia has been identified in six eastern and central European countries (Poland, Germany, Czechia, Hungary, Romania and Slovakia) since the end of December 2019. In the same period, two subtypes with different genetic characteristics were reported in Bulgaria: i) an HPAI A(H5N8) descendant of the A(H5N8) strain introduced into Europe in 2016 and ii) a reassortant HPAI A(H5N2) between the Bulgarian A(H5N8) and Eurasian LPAI viruses. • In contrast to the last reporting period, no HPAI outbreaks were notified from Africa and a decreasing number of outbreaks of HPAI A(H5N1), A(H5N2), A(H5N5), A(H5N6) and A(H5N8) in poultry and wild birds were notified from Asia and the Middle East. • The risk of zoonotic transmission of AI viruses to the general public in Europe remains very low. No transmission to humans has been observed related to viruses detected in Europe over the last few months; however, the evolution of AI viruses and recent reassortment events need to be closely monitored. • The first European A(H5N8) outbreak was reported in poultry on 30 December 2019 and remained confined to a few countries in eastern and central Europe. Some of the possible explanations for this localised epidemic wave are i) the late virus introduction; ii) a different route of virus spread; iii) a mild winter; and iv) the spring migration. • Only five of the 263 poultry outbreaks detected in Hungary were primary, suggesting that the spread of the virus was mainly due to secondary spread and not to multiple introductions from wild birds. • The genetic analysis of the HPAI A(H5N8) viruses that have been isolated from Poland, Czechia, Germany, Hungary, Romania and Slovakia since December 2019 indicates that the virus is a reassortant between HPAI A(H5N8) viruses from Africa and LPAI viruses from Eurasia. • The genetic analysis conducted on the HPAI A(H5N2) and A(H5N8) viruses isolated in Bulgaria suggest a persistence of the virus in the country since 2016 rather than a new introduction via migratory wild birds. • The long persistence of the virus in a few countries may pose a risk for the emergence of new reassortant viruses and be a source of virus spread to wild or domestic birds in the EU/EEA Member States. • There were a low number of HPAI cases identified in wild birds in this 2019-2020 epidemic season in Europe. There may be several explanations for this low numbers: i) the relatively high temperatures may have determined changes in westward and southward movement of migratory birds coming from Asiatic countries; ii) the effort of passive surveillance activities might not be enough to detected infected wild birds if the prevalence of the infection is low as it might have been this year; iii) a reduction of surveillance activities due to the COVID-19 epidemic; iv) an increased resistance against the disease due to a herd immunity of wild birds following past seasonal exposures to AI A(H5); v) difficulty of the current surveillance system to identify infected migratory birds coming through unusual migratory flyways. At present, data are not sufficient to confirm what is being assumed. More time and further studies are needed to confirm these hypotheses. • Despite the decreasing number of HPAI A(H5)-affected countries and outbreaks outside Europe, there is considerable uncertainty regarding the real geographical distribution of these viruses. • Continued surveillance for AI virus in wild birds and poultry in Europe and worldwide, combined with timely generation of complete viral genome sequences and data sharing among European countries and between animal and human health sectors, are crucial in order to be able to detect and respond promptly to threats that are relevant to animal and public health. • It is particularly important that information on the genetic composition and possible origins of newly detected variants in birds and humans are shared and communicated in a timely manner. • The high number of secondary spreads recorded in duck and goose establishments in some countries, such as Hungary, indicates that these types of poultry category need to be better regulated to increase biosecurity and to prevent uncontrolled spread of infection. • A better understanding of the factors regulating wild bird migration is of the utmost importance to improve our ability to detect the virus early and monitor its spread. • A more effective surveillance (economically sustainable) that considers the new epidemiological scenarios of HPAI viruses in wild birds should be designed and implemented. • Due to the difficulty of predicting and identifying the spread of HPAI viruses in their natural reservoirs, high standard alert, effective biosecurity measures particularly during high risk periods such as the winter season, and the ability of the poultry industry to adapt production systems according to the risk assessment (e.g. free-range birds kept indoors in situations considered to be at high risk) are still the main preventive tools against HPAI in Europe. Figure 1 shows the HPAI outbreaks detected in birds (poultry, wild and captive birds) in Europe and reported via ADNS for seasons 2016-2017, 2017-2018, 2018-2019 and 2019-2020 . Figure 2 shows the same data only for the last three epidemic seasons. A season is the period that starts in week 40 (the beginning of October) and ends in week 39 (the end of September) of the following year. For the current season, 2019-2020, data reported are truncated at the middle of week 20 (on 15 May 2020), as the season is still ongoing. As of 22 June 2020, a number of HPAI outbreaks have been confirmed in poultry outside the reporting period for this report: one in Bulgaria on 4 June 2020 and six in Hungary between 18 May and 4 June 2020. An LPAI A(H5N3) outbreak was confirmed outside the reporting period for this report, on 16 June 2020, in an ostrich establishment located in Mantova province, Italy. Number of HPAI-affected establishments by poultry species and production category in the EU, 16 February -15 May 2020 (n=287). Number of HPAI-affected establishments in the EU from 16 February -15 May 2020, according to the commercial type and the number of susceptible bird species bred (n=287) HPAI A(H5N2) and A(H5N8)-affected poultry establishments in Bulgaria Between 20 February and 3 March 2020, three HPAI A(H5N2) and four HPAI A(H5N8) outbreaks were detected at poultry establishments in two regions in Bulgaria. Six of those were detected in Plovdiv Region and only one in Kardjali. The last outbreak detected in Plovdiv was a secondary outbreak. The characteristics of the affected establishments and species reared are presented in Table 2 . On 17 February, one HPAI A(H5N8) outbreak was detected at a mixed poultry establishment in Pardubice Region in Czechia. Mortality, clinical signs and a drop in feed/water intake were detected in turkeys; no signs of AI infections were reported in the broilers. Indirect contact with wild birds was mentioned as the most likely source of infection. The characteristics of the affected establishment and species reared are presented in Table 2. HPAI A(H5N8)-affected poultry establishments in Germany On 20 and 27 February 2020, two HPAI A(H5N8) outbreaks were detected at poultry establishments in Aurich and Borde regions, respectively, in Germany. The outbreak in Aurich was identified in a breeding turkey establishment in an area close to a wild bird resting place; the one in Börde in a fattening turkey establishment in the direct neighbourhood of a large river. The epidemiological investigations of both outbreaks identified indirect contact with wild birds as the most likely source of infection. Characteristics of the affected establishments and species reared are presented in Table 2. HPAI A(H5N8)-affected poultry establishments in Hungary Between 22 March and 12 May 2020, 263 HPAI A(H5N8) outbreaks were detected at poultry establishments in Báca-Kiskun, Békés and Csongrád regions in Hungary ( Figure 12 ). Five of the outbreaks were reported to be primary outbreaks, and the rest were secondary outbreaks with some of these secondary outbreaks related to other secondary outbreaks. There were eight mixed species establishments and the rest all house only one species. In total, 31 establishments did not record any signs of infections, while the other 232 establishments did (figure 12). One establishment reported the source of infection to be unknown, two establishments reported it to be indirect contact with wild birds, and all the rest reported the source of infection to be indirect contact with poultry. None of the establishments reported having outdoor access. Of all the establishments, only 12 were reported as non-commercial; the rest were commercial. The characteristics of the primary affected establishment and species reared are presented in Table 2 . Between 20 February and 30 March 2020, 14 HPAI A(H5N8) outbreaks were detected at poultry establishments in 12 regions in Poland. Of those, one establishment reared mixed bird species (domestic duck, domestic goose and chicken); it was detected via outbreak-related surveillance as secondary to an outbreak reported in the previous EFSA report (EFSA et al., 2020) with the most likely source of infection being indirect contact with poultry. For all the other outbreaks identified by means of outbreakrelated surveillance, the same transport company which delivered duckings was involved in the spred of the virus among those establishemnts. Indirect contact with wild birds was reported as the most likely source of infection for a duck establishment and the chicken establishment, in the latter the animals had access to an outdoor river. For the two turkey establishments the most likely source of infection was unknown. Characteristics of the affected establishments and species reared are presented in Table 2 . Information extracted from the scientific literature A HPAI A(H5N8) virus infection (Ger-01-20) was detected in chickens in Baden-Wuerttemberg, Germany on 6 February 2020. It was a reassortant with six gene segments closely related to the 2.3.4.4b clade of the gs/Gd lineage of HPAI (H5), and the gene segments coding for PB1 and NP closely related to a LPAI A(H3N8) virus circulating in wild waterbirds in central Russia. At gross autopsy, the birds showed moderate mucous discharge in the upper respiratory tract and diarrhea. By histopathology, they had a severe acute diffuse necrotizing lymphohistiocytic enteritis and a moderate necrotizing encephalitis with perivascular cuffing and gliosis (King et al., 2020) . Between 16 February and 15 May 2020, one HPAI case in wild birds was notified in Europe (Table 3) . It was HPAI A(H5N8) virus in a common buzzard (Buteo buteo) found dead near Leipzig, Germany, on 21 March, a few days after HPAI A(H5N8) virus was detected on 12 March in a non-commercial establishment of chickens in the same area. Information extracted from the scientific literature The same Ger-01-20 reassortant that was detected in chickens (see 4.2.2.1) was detected in a greater white-fronted goose (Anser albifrons) that was found dead close to the Polish border in the federal state of Brandenburg, Germany on 16 January 2020. Although the proximate cause of death was trauma, the ultimate cause of death was considered to be a severe necrotizing polioencephalitis associated with the virus infection, which most likely causing disorientation and predisposed the goose to the traumatic event (King et al., 2020) . Between 16 February and 15 May 2020, two LPAI outbreaks were notified in the poultry sector in Europe; two A(H7N1) in Italy. Information available from the ADNS (European Commission, online-a), from the OIE (OIE, online) and provided by Member States characterising the LPAI outbreak is presented in Table 4 . The two affected establishments were located adjacent to each other. LPAI infected animals showed only very mild respiratory symptoms. The most likely source of virus entrance was identified as indirect contact with wild birds; the establishments were in proximity to wetlands where wild birds (e.g. herons, ducks) were present. Description of the nomenclature of the HPAI A(H5) viruses used in the document Phylogenetic analyses identified the circulation of viral genotypes showing three distinct gene constellations ( Figure 14 ). Specifically, HPAI A(H5N8) viruses from Poland, Czechia, Germany, Hungary, Romania and Slovakia cluster together for all the eight gene segments. This genotype was generated through reassortment events between HPAI A(H5N8) viruses from Africa and LPAI viruses from Eurasia, as described in the previous report (EFSA et al., 2020; King et al., 2020; Świętoń et al., 2020) . The HPAI A(H5N8) viruses from Bulgaria cluster separately from the A(H5N8) viruses currently circulating in eastern and central Europe. They belong to the previously defined A/mute swan/Croatia/70/2016-like genotype Four out of the eight HPAI outbreaks identified in Bulgaria from February 2020 were caused by an A(H5N2) subtype arising from reassortment events between the HPAI A(H5N8) from Bulgaria and the LPAI viruses identified in wild and domestic birds in Eurasia. To date, there is no evidence of mutations associated with mammalian adaptation in any of the analysed viruses. Analyses were based on sequence data: a) deposited in GISAID; b) donated by Member States via the EURL network; and c) produced by the EURL (IZSVe) from submitted viruses. Genetic characterisation of LPAI viruses of the A(H7) subtype circulating in Europe The genomes of the two LPAI A(H7N1) viruses identified in two contiguous turkey farms (same epidemiological unit) in Italy are highly related. The HA gene of the two viruses shares a common progenitor with a LPAI A(H7N3) virus identified in chicken of a poultry dealer in Italy in July 2019, while the remaining gene segments cluster with those of contemporary viruses from Eurasian wild birds. Such data suggest the occurrence of a single introduction from wild birds rather than the undisclosed maintenance of the virus in poultry populations. No human infection with A(H5N2) or A(H5N8) viruses, as detected in wild birds and poultry in Europe, has been reported during the period covered by this report or been previously reported (EFSA et al., 2020) . A risk assessment on A(H5N8) is available from WHO stating that the likelihood of human infection with A(H5N8) virus is low (WHO, online). Of the 410 people (Table 2) exposed during the recent outbreaks, no transmission of avian influenza has been reported. An overview of the HPAI outbreaks notified from other countries not reporting via ADNS but via the OIE or national authorities from 16 February to 15 May 2020 is presented in Table 5 and Figure 15 . For the purposes of this report, only findings of AI viruses occurring in countries that are considered to be of epidemiological interest for the EU/EEA or of public health relevance are described. During the reporting period, no new relevant information concerning mammals (humans excluded) has been published on the phenotypic and genetic characterisation of HPAI A(H5N1) viruses circulating in countries outside the EU/EEA. No new human case due to AI A(H5N1) has been reported since the last report (EFSA et al., 2020) . The Taiwanese lineage HPAI A(H5N2) has been in circulation in Taiwan since 2012 and caused severe outbreaks at chicken, duck, goose and turkey establishments. In the relevant time period for this report Taiwan detected four new outbreaks of HPAI A(H5N2) on medium-sized poultry farms and one case was confirmed on a large chicken farm ( Figure 18 ). The Taiwanese During the reporting period, no new relevant information concerning mammals (humans excluded) has been published on the phenotypic and genetic characterisation of HPAI A(H5N6) viruses circulating in countries outside the EU/EEA. No new human case due to AI A(H5N6) has been notified since the last EFSA report ( No human cases due to AI A(H7N9) have ever been reported from Europe and no human case has been reported globally since the last EFSA report (WHO, 2020c, a). Since February 2013, a total of 1,568 human cases have been reported from outside of Europe ( Information extracted from the scientific literature Li et al. (2020) characterised an LPAI A(H9N2) virus isolated in December 2017 in China, from an unidentified migratory wild waterbird species. This virus was a reassortant carrying PB1, HA and NA gene segments closely related to North American lineage wild-bird-origin LPAI viruses, while the other gene segments were related to various LPAI viruses isolated in China or Japan. Haemagglutination tests against different types of red blood cells indicated that this strain possessed an avian-like α-2,3-linked sialic acid receptor specificity. The H9 sequence had a monobasic cleavage site sequence characteristic of avian influenza viruses with low pathogenicity in chickens, and the PB2 sequence did not possess previously described major substitutions associated with adaptation to mammalian hosts. Although mutations in the M1 and NS1 sequences were observed that suggested an enhanced virulence in mice, in vivo intranasal inoculation in 6-week-old female BALBc mice with doses varying from 10 to 106 EID50 only induced a transient loss of weight at 3 days post-inoculation, which was compensated for at 14 days post-inoculation when compared with uninfected control mice. At 3 days post-inoculation, virus was not detected from brain, spleen, kidney, lung or the nasal turbinate tissues of mice inoculated with the highest 106 EID50 dose. In vivo studies therefore indicated low pathogenicity of this A(H9N2) in mice. and June 2019. The in vitro infectivity in MDCK cells and in vivo pathogenicity in 6-week-old BALB/c mice, following intranasal inoculation of a 106 EID50 viral dose, were variable. Only some of the tested A(H9N2) strains were able to replicate in mouse lung tissues and to induce alveolar tissue damage and body weight loss after inoculation. In this last case, weight loss was, at most, slightly more than 10% and was compensated for by the end of the 13-day observation period: for all tested A(H9N2) viruses, no mortality was observed and final body weights were equivalent to the control group. Although nine amino acid substitutions in five genome segments are here described as correlating with enhanced replication or pathogenicity in mice, their contribution remains to be elucidated. Since the last EFSA report, four new human cases have been reported from China: one in a 3-year-old girl with onset of symptoms on 22 March 2020 in Guangdong Province, China; a second in a 5-year-old girl from Hunan Province with onset of symptoms on 20 April 2020; a third on 4 May 2020 in a 10-month-old boy in Xiamen, Fujian Province and a fourth case in a 6-year-boy from Weihai, Shandong Shen (WHO, 2020a; Taiwan Centers for Disease Control Press Releases, online). The recent slight increase in reported human cases due to A(H9N2) could be related to an intensified testing of all people with respiratory symptoms due to the ongoing COVID-19 pandemic. All cases reported exposure to domestic poultry or slaughtered poultry. Since 1998, and as of 15 May 2020, 66 laboratory-confirmed cases of human infection with AI A(H9N2) virus, including one death, have been reported globally. Cases were reported from China (55) Possible pathways by which AI viruses can be brought into the EU have been described in previous EFSA reports (EFSA AHAW Panel, 2017; EFSA et al., 2018a; EFSA et al., 2018b) . In contrast to the last report (EFSA et al., 2020) 4.6.1. The measures outlined in the EFSA report for November 2017 -February 2018 (EFSA et al., 2018c) remain valid. In February 2020, a new candidate vaccine virus for A(H9N2) (WHO, 2020e) based available antigenic, genetic and epidemiologic data, A/Oman/2747/2019-like A(H9N2), was proposed. The risk of zoonotic influenza transmission to the general public in EU/EEA countries remains very low, although an increasing number of outbreaks due to AI viruses has been reported in Europe. Transmission to humans of AI viruses, detected in wild birds or poultry in Europe, has not been observed recently. However, zoonotic transmission of AI viruses cannot be fully excluded in general when AI viruses are present in birds. The use of personal protective measures for people exposed to AI viruses will minimise any residual risk. Overall, AI virus transmission to humans is a rare event and the risk is considered to be very low for viruses adapted to avian species. The risk of travel-related importation of human AI cases, particularly from Asia, is very low. Currently, only a few sporadic outbreaks in birds and poultry are reported worldwide. Sporadic human cases infected with A(H9N2) LPAI viruses underline the risk of transmission whenever people are exposed to infected birds in countries where A(H9N2) is endemic. Therefore, surveillance of AI viruses in wild birds and poultry in the EU/EEA is important in order to detect newly introduced and circulating viruses and reduce the possible risk of exposure of humans to infected birds. Avian influenza is an infectious viral disease in birds, including domestic poultry. Infections with avian influenza viruses in poultry cause two main forms of that disease that are distinguished by their virulence. The low pathogenic (LPAI) form generally only causes mild symptoms, while the highly pathogenic (HPAI) form results in very high mortality rates in most poultry species. That disease may have a severe impact on the profitability of poultry farming. Avian influenza is mainly found in birds, but under certain circumstances infections can also occur in humans even though the risk is generally very low. More than a decade ago, it was discovered that virus acquired the capability to be carried by wild birds over long distances. This occurred for the HPAI of the subtype A(H5N1) from South East and Far East Asia to other parts of Asia, Europe and Africa as well as to North America. In the current epidemic the extent of the wild bird involvement in the epidemiology of the disease is exceptional. Since late October 2016 up to early February 2017, highly pathogenic avian influenza (HPAI) of the subtype A(H5N8) has been detected in wild migratory birds or captive birds on the territory of 21 Member States, namely Austria, Belgium, Bulgaria, Croatia, Czechia, Denmark, Finland, France, Germany, Greece, Hungary, Ireland, Italy, the Netherlands, Poland, Portugal, Slovakia, Slovenia, Spain, Sweden and the United Kingdom. In 17 Member States the virus has spilled over to poultry holdings leading also to lateral spread between holdings in a few Member States, in particular in those with a high density of duck and geese holdings where the poultry cannot sufficiently be protected against contacts with wild birds. A second HP AI subtype A(H5N5) has been detected in wild birds and recently also in poultry holdings in Germany. The number of infected migratory wild birds found dead and the geographical extent of these findings are posing an immense threat for virus introduction into poultry or captive birds holdings as demonstrated by the high number of outbreaks (~700 as of 08/02/2017). In the event of an outbreak of avian influenza, there is a risk that the disease agent might spread to other holdings where poultry or other captive birds are kept. As a result it may spread from one Member State to other Member States or to third countries through trade in live birds or their products. There is knowledge, legislation 2 , technical and financial tools in the EU to effectively deal with outbreaks of avian influenza in poultry and captive birds. However, the very wide virus spread by wild birds and the increased risk of direct or indirect virus introduction into poultry or captive bird holdings has led to the largest HPAI epidemic in the EU so far. This situation calls for a reflection and evaluation how preparedness, risk assessment, early detection and control measures could be improved. The Commission and Member States are therefore in need of an epidemiological analysis based on the data collected from the disease affected Member States. The use of the EFSA Data Collection Framework is encouraged given it promotes the harmonisation of data collection. Any data that is available from neighbouring third countries should be used as well, if relevant. Analyse the epidemiological data on highly pathogenic avian influenza (HPAI) and low pathogenic avian influenza (LPAI), where co-circulating or linked within the same epidemic, from HPAI disease affected Member States. Analyse the temporal and spatial pattern of HPAI and LPAI as appropriate in poultry, captive birds and wild birds, as well the risk factors involved in the occurrence, spread and persistence of the HPAI virus in and at the interface of these avian populations. Based on the findings from the points above, describe the effect of prevention and control measures. Provide for regular quarterly reports updating on the avian influenza situation within the Union and worldwide, in particular with a view to describe the evolution of virus spread from certain regions towards the EU. In case of significant changes in the epidemiology of avian influenza, these reports could be needed more frequently. These reports should in particular closely follow the developments of zoonotic avian influenza viruses (such as HPAI A(H5N6) and LPAI A(H7N9)) in collaboration with the European Centre for Disease Prevention and Control (ECDC). In reply to TOR 1 and TOR 2, this scientific report gives an overview of the HPAI and LPAI outbreaks in poultry, captive and wild birds detected in Europe between 16 February and 15 May 2020 and reported by Member States and neighbouring countries via ADNS. Member States where avian influenza (AI) outbreaks occurred in poultry submitted additional epidemiological data to EFSA, which have been used to analyse the characteristics of the affected poultry establishments. It was not possible to collect data for a risk factor analysis on the occurrence and persistence of HPAI virus within the EU. Risk factor analysis requires not only case-related information, but also data on the susceptible population (e.g. location of establishments, population structure), which should be collected in a harmonised manner across the EU. Limitations in the data collection, reporting and analysis were explained in the first AI overview report (EFSA AHAW Panel, 2017). If HPAI outbreaks in poultry are detected in the EU, a description of the applied prevention and control measures (TOR 3) is given in the case report provided by representatives from the affected Member States and attached as an annex. The main topics covered are increasing awareness, release and repeal of housing orders, strengthening biosecurity, preventive culling, implementation of a regional standstill, bans on hunting and derogations from restriction zone implementation after a risk assessment. Monitoring of the AI situation in other countries (TOR 4) is based on data submitted via the OIE or reported to the FAO. The description focuses only on findings of AI viruses occurring in countries that are considered to be of epidemiological interest for the EU/EEA or of public health relevance, specifically on HPAI A(H5N1), HPAI A(H5N2), HPAI A(H5N5), HPAI A(H5N6), HPAI A(H5N8), HPAI/LPAI A(H7N9) and LPAI A(H9N2). The background and epidemiology, detections, phenotypic and genetic characterisations are described based on information from confirmed human, poultry and wild bird cases that occurred between 16 Februay and 15 May 2020 and on information gathered by performing a literature search on papers published in PubMed from 16 February to 15 May 2020. Possible actions for preparedness in the EU are discussed. This report mainly describes information that became available since the publication of the EFSA report for the period November 2019 -February 2020 (EFSA et al., 2020) and that might affect the interpretation of risks related to AI introduction and/or spread in Europe. samples have been taken (mainly at live market-places) will not move around and not spread the infection by migrating and for this reason have been considered as domestic birds in the maps provided in this report. Only when there was a strong discrepancy between the locality, the administrative regions and geocoordinates, and the outbreaks were not officially reported to the OIE, were the confirmed outbreaks not taken into account in the analysis. Information on phenotypic and genotypic characterisation of HPAI viruses circulating on other continents and in other regions (Africa, Asia, the Middle East) in domestic or wild birds or mammals (excluding humans) were extracted from the scientific literature by performing a literature review. Review questions Update on the phenotypic and genetic characterisation of HPAI viruses circulating on other continents and in other regions (Africa, Asia, the Middle East) in domestic or wild birds or mammals (excluding humans) within the last three years. Search The PubMed database was searched by using subject index terms and free-text terms combined with the appropriate Boolean operators. Scientific articles added to the database between 16 February and 15 May 2020 were searched; the search was run on 17 February 2020. Relevance criteria Scientific articles added to the database between 16 February and 15 May 2020 that report information on the presence or absence of clinical signs, pathological changes or mortality or genotypic characterisation (only new information) due to HPAI infection with viruses circulating within the last three years in Asia, Africa or the Middle East in domestic or wild birds or mammals other than humans. Eligibility criteria Host species all domestic birds or wild birds present in the EU or mammals other than humans; the virus subtype should be reported; for experimental studies only the age of the infected animals should be reported (at least as juvenile/adult). The search retrieved 118 papers. The articles were subsequently screened against the relevance and eligibility criteria. Seven papers were in the end taken into consideration in the description of phenotypic and genotypic characterisation of HPAI viruses circulating on other continents and in other regions (Africa, Asia, the Middle East) in domestic or wild birds or mammals (excluding humans) in the reporting period. The search protocol and the results can be consulted at https://doi.org/10.5281/zenodo.3908523. The numbers of human cases due to infection with AI viruses have been collected by ECDC. Multiple sources are scanned regularly as part of epidemic intelligence activities at ECDC to collect information about laboratory-confirmed human cases. Data were extracted and line lists developed to collect casebased information on virus type, date of disease onset, country of reporting, country of exposure, sex, age, exposure, clinical information (hospitalisation, severity) and outcome. All cases included in the line list and mentioned in the document have been laboratory-confirmed. Data are continuously checked for double entries and validity. The data on human cases cover the full period of time since the first human case was reported. Therefore, data on human cases refer to different time periods and are included irrespective of whether there have been any new human cases during the reporting period. Scope This document provides a brief overview of the specific prevention and control measures applied in Bulgaria, Czechia, Hungary and Poland between 16 February and 15 May 2020 in relation to HPAI outbreaks in poultry. Information is only provided if it is considered relevant to the implementation of the following selected measures: increasing the awareness of stakeholders and the general public, housing orders, strengthening biosecurity measures (other than poultry confinement), preventive culling, regional stand still, derogations from restriction zone implementation after risk assessment and hunting ban. This document is prepared to support the EFSA working group in generating an overview on the application of the selected measures at EU level. Tables A.1-A.4 provide timelines for the main events that triggered actions in relation to the selected prevention and control measures in Bulgaria, Czechia, Hungary and Poland. More information on the actions taken is provided in the sections below the tables. Animal Health and Welfare, and Feed Control Directorate -Bulgarian Food Safety Agency Reorganisation of the duck sector -the whole technology cycle/life to be in one holding or different but technologically linked and belonging to the same owner/company/operator. This measure aims at decreasing the movement of ducks from farm to farm and avoiding one farm (gavage) to be used by different owners/companies. Transport of ducks -separate transport means to be used for ducks and Galliformes. GPS equipment for all poultry transport in order to allow the traceability of poultry movement. Established a sanitary period of at least 21 days (one incubation period) -a ban on restocking of all duck farms in Bulgaria (2.05.2020 -28.05.2020) and on slaughtering ducks (24.07.2020 -23.08.2020 ). During the sanitary periods, cleaning and disinfection of all premises will be carried out. The duck farms will be inspected for compliance with biosecurity rules by an Expert Commission requiring positive results before restocking. This sanitary period shall be implemented every year as the period to be fixed additionally. Enhanced laboratory surveillance, as follows: -official control and serology/virology sampling of poultry in backyards located in risk areas (areas with high density of poultry holdings and areas with high population of migratory wild birds) -routine official control four times per year at least in duck farms and serology sampling of all flocks at 45-65 days old present in the farm at the time of the visit. The official control will replace the current self-control. Increased official inspections ensuring the implementation of the biosecurity measures in poultry farms -twice per year in the risk areas mentioned above (in the duck sector these checks to be part of the inspections related to the laboratory surveillance). Increasing awareness of the stakeholders and the general public 1. Regular meetings with representatives of the poultry associations; a number of the measures such as increased control and surveillance, were proposed by the poultry industry sector itself. The sector is actively engaged and thoroughly cooperates in implementing the control and surveillance activities. 2. Close cooperation with the public health authority. 3. Publishing information related to the epidemiological situation and prevention and control measures taken: http://www.babh.government.bg/bg/Page/influentza/index/influentza/%D0%98%D0%BD%D1%84% D0%BB%D1%83%D0%B5%D0%BD%D1%86%D0%B0%20%EF%BF%BD Continuing the enforcement of the measures as described in the previous scientific report. Measures as described in the previous scientific report. Not applied. Not applied. Not applied. Not forbidden. Lucie Kalášková, Milada Dubská Department of Animal Health and Animal Welfare State Veterinary Administration of the Czech Republic Information about the second outbreak of highly pathogenic avian influenza (HPAI) in Czechia On 16 February 2020 the State Veterinary Administration in Pardubice Region received information about higher mortality among turkeys on a commercial farm with turkeys, broilers (Gallus Gallus) and pigs. At the same time, the official vets visited this holding and took samples from dead birds for laboratory testing. The samples were sent to the State Veterinary Institute in Prague (SVI Prague) -National Reference Laboratory (NRL) for Avian Influenza, which confirmed the presence of HPAI subtype H5N8 by PCR on 17 February 2020. On 17 February 2020 the emergency veterinary measures were in place in accordance to the Council Directive 2005/94/EC introducing Community measures for the control of avian influenza. The emergency veterinary measures included culling of all remaining poultry, safe disposal of poultry products, feed stuffs and by-products and preliminary cleaning and disinfection. The emergency veterinary measures for the protection and the surveillance zone were taken in line with EU legislation. The final cleaning and disinfection was carried out on 12 March 2020. The surveillance zone around the outbreak was lifted on 23 March 2020. The release of poultry (pheasant, mallard) and other captive birds for restocking purpose was forbidden inside the restricted zone (emergency veterinary measure) established around the outbreak. National Food Chain Safety Office Increasing awareness, release housing order, preventive culling, regional stand still, derogations on restriction zone implementation after risk assessment 5. -31/03/2020 First poultry outbreak in Csongrád County in 2020 -30/04/2020 First poultry outbreak in Békés County in 2020 - All information about avian influenza is available on the website of the National Food Chain Safety Office: https://portal.nebih.gov.hu/madarinfluenza The Chief Veterinary Officer (CVO) and head of the National Disease Control Center has communicated the most important information about the epidemic to the national media. On 16 January 2020 the 1/2020 CVO Decision entered into force which ordered the closed keeping of poultry (including backyard) in the whole country: https://portal.nebih.gov.hu/documents/10182/1294174/OFA+hat%C3%A1rozat+1-2020.pdf/df9982e7-8e12-908d-c30a-866902ecb0fc The 3/2017 CVO Decision about strengthening biosecurity requirements has been in force since the 2016/2017 HPAI epidemic; no additional measures have been introduced yet. Preventive killing/slaughter has been carried out -based on a risk assessment -in protection zones and also in certain parts of the surveillance zones. In the whole territory of the affected counties: transport of poultry can only take place after a negative PCR result. No stocking can take place in the restricted zones. As additional measures to control the HPAI spread, the radius of the surveillance zones have been enlarged based on the density of poultry establishments and of the administrative boundaries in some areas. This was the case in Bács-Kiskun and Csongrád-Csanád county (where most of the outbreaks were) and in Békés county ( Figure A. 3.1) Based on risk assessment in accordance with to Council Directive 2005/94/EC, poultry was transported out of the surveillance zone after laboratory examination to immediate slaughter. Hunting EFSA Journal 2020;18(6): 6194 Not restricted. No special rules apply. General Veterinary Inspectorate suspicions and the national control programme in relation to AI Information is published on the website of the General Veterinary Inspectorate: https://www.wetgiw.gov.pl/nadzor-weterynaryjny/grypa-ptakow Requirements in the field of biosecurity applicable to poultry breeders throughout the country are set out in the Regulation of the Minister of Agriculture and Rural Development of 4 April, 2017 on the ordinance of measures related to the occurrence of highly pathogenic avian influenza. This regulation imposes the following obligations on breeders: • an order to keep poultry in a way that limits their contact with wild birds, • reporting to the District Veterinary Officer places where poultry or other birds are kept, excluding birds kept permanently in living quarters, • keeping the poultry in a way that excludes its access to water bodies to which wild birds have access, • storing bird feed in a way that prevents contact with wild birds and their droppings, • feeding and watering poultry and captive birds in a manner that protects feed and water from access by wild birds and their droppings, • laying disinfection mats in front of the entrances and exits of livestock buildings in which poultry are kept, in a number ensuring the security of entrances and exits from these buildings -in the case of farms where poultry is kept in a non-running system, • use of protective clothing and safety footware by persons entering livestock buildings in which poultry are held, intended for use only in the given building -in the case of farms where poultry are kept in a non-running system, • personal hygiene rules applied by persons performing poultry handling operations, including washing hands before entering livestock buildings, • cleaning and disinfection of equipment and tools used for handling poultry before each use, • abstentions by persons who have participated in the hunting of birds in the last 72 hours from carrying out poultry-handling activities, • carrying out daily inspections of poultry flocks and keeping records containing, in particular, information on the number of dead birds, decrease in feed intake or lay, • a ban on watering poultry and birds kept by humans with water from tanks to which wild birds have access, and • a ban on bringing (on foot or by vehicle) to the holding where poultry is kept, corpses of wild birds or carcasses of game birds. The Regulation of the Minister of Agriculture and Rural Development of 4 April, 2017 regarding the ordinance of measures related to the occurrence of HPAI introduced into the territory of the Republic of Poland, among others, issues an order to keep the poultry in a way that limits its contact with wild birds or to store feed for birds in a way that prevents contact with wild birds and their droppings. The measures specified in the provisions of this Regulation are also applied during outbreaks of HPAI in the territory of the Republic of Poland. Spatial spread and emergence of reassortant H5 highly pathogenic avian influenza viruses in Iran reassortant H5 highly pathogenic avian influenza virus in Iran Outbreaks of Clade 2.3.4.4 H5N8 highly pathogenic avian influenza in 2018 in the northern regions of South Africa were unrelated to those of 2017 Estimation of the number of exposed people during highly pathogenic avian influenza virus outbreaks in EU/EEA countries Isolation and Characterization of Avian Influenza H9N2 Viruses from Different Avian Species in Pakistan 2016-17 Avian influenza H9N2 subtype in Ghana: virus characterization and evidence of co-infection A G1-lineage H9N2 virus with oviduct tropism causes chronic pathological changes in the infundibulum and a long-lasting drop in egg production A Well-Defined H9N2 Avian Influenza Virus Genotype with High Adaption in Mammals was Prevalent in Chinese Poultry Between WHO Collaborating Center for Reference and Research on Influenza and National Institute for Viral Disease Control and Prevention China Characterization of H9N2 avian influenza viruses from the Middle East demonstrates heterogeneity at amino acid position 226 in the hemagglutinin and potential for transmission to mammals Scientific Report: Avian influenza overview Scientific Report: Avian influenza overview Scientific Report: Avian influenza overview Scientific Report: Avian influenza overview Scientific Report: Avian influenza overview Scientific Report: Avian influenza overview Animal Disease Notification System (ADNS) European Commission, online-b. Animal Health -Regulatory Committee presentations online-a. H7N9 situation update FAO (Food and Agriculture Organization), online-b. EMPRES-i -Global Animal Disease Information System Genetic Diversity of Highly Pathogenic Avian Influenza A(H5N8/H5N5) Viruses in Italy Preliminary Epidemiologic Assessment of Human Infections With Highly Pathogenic Avian Influenza A(H5N6) Virus, China Antigenic Variant of Highly Pathogenic Avian Influenza A(H7N9) Virus, China Genetic characterization and pathogenesis of the first H9N2 low pathogenic avian influenza viruses isolated from chickens in Kenyan live bird markets Novel HPAIV H5N8 Reassortant (Clade 2.3.4.4b) Detected in Germany Evolution, global spread, and pathogenicity of highly pathogenic avian influenza Characterization of a novel reassortant H5N6 highly pathogenic avian influenza virus clade 2.3.4.4 in Korea Death of a very young child infected with influenza A (H5N6) Novel Reassortant Avian Influenza A(H9N2) Virus Isolate in Migratory Waterfowl in Hubei Province OIE (World Organisation for Animal Health), online. World Animal Health Information Database (WAHIS) Interface Active virological surveillance in backyard ducks in Bangladesh: Detection of avian influenza and gammacoronaviruses A Global Perspective on H9N2 Avian Influenza Virus Laboratory-confirmed avian influenza A(H9N2) virus infection Cumulative number of confirmed human cases for avian influenza A(H5N1) reported to WHO Antigenic and genetic characteristics of zoonotic influenza A viruses and development of candidate vaccine viruses for pandemic preparedness Phylogenetic classification of hemagglutinin gene of H9N2 avian influenza viruses isolated in China during 2012-2016 and evaluation of selected candidate vaccine strains Influenza A(H9N2) Virus, Burkina Faso Genetic characteristics of H9N2 avian influenza viruses isolated from free-range poultry in Eastern China Data on the AI outbreaks that occurred in Europe from 16 February to 15 May 2020 submitted by Member States to the ADNS (European Commission, online-a) were taken into account for this report.In addition, HPAI affected Member States were asked to provide more detailed epidemiological data directly to EFSA on the AI outbreak that occurred in poultry during the same period.The information, which EU Member States affected by HPAI and LPAI presented to the Standing Committee on Plants, Animals, Food and Feed (SCOPAFF) meetings, and the evidences on HPAI and LPAI outbreaks provided in the info notes from the affected Member States to the European Commission, were consulted to extract the relevant information which is reported in Section 4.2.2. The PDFs of the SCOPAFF presentations are available on the European Commission website (European Commission, online-b).The public GISAID's EpiFlu™ Database was accessed to download newly released avian influenza sequences.A descriptive analysis of the data collected is reported in Section 4.2. Information on the phenotypic characterisation of AI viruses circulating in the EU was extracted from the scientific literature by performing a literature review.Review question Update on the phenotypic characterisation of HPAI viruses circulating in the EU in domestic and wild birds within the last two years.Search The PubMed database was searched by using subject index terms and free-text terms combined with the appropriate Boolean operators. Scientific articles added to the database from 16 February to 15 May 2020 were searched; the search was run on 17 February 2020.Relevance criteria Scientific articles added to the database from 16 February to 15 May 2020 and reporting information on the presence or absence of clinical signs or pathological changes or mortality due to HPAI infection with viruses circulating within the last two years in the EU in domestic or wild birds.Eligibility criteria Host species all domestic birds or wild birds present in the EU; the virus subtype should be reported; for experimental studies only, the age of the infected animals should be reported (at least as juvenile/adult). The search retrieved 140 papers. The articles were subsequently screened against the relevance and eligibility criteria. One of the screened papers was in the end taken into consideration in the description of the phenotypic characterisation of HPAI viruses circulating in the EU in domestic and wild birds in the reporting period.The search protocol and the results can be consulted at https://doi.org/10.5281/zenodo.3908523. Data from FAO EMPRES-i (FAO, online-b) on HPAI A(H5N1), HPAI A(H5N2), HPAI A(H5N5), A(H5N6), A(H5N8), HPAI and LPAI A(H7N9) in domestic, captive and wild birds, and environmental samples, were used to describe and to map the geographical distribution of AI cases in domestic and wild birds in Africa, Asia, the Middle East and Europe on the basis of the observation dates. Data were extracted on 11 June 2020. With the purpose of avoiding over-complication of the maps, captive birds and environmental samples have been mapped as domestic birds. Although some of these kept animals may be wild species, in most of the cases captive birds, or, for environmental samples, the birds from which On the website of the State veterinary administration was regularly updated with information about avian influenza situation in 2018 -https://www.svscr.cz/zdravi-zvirat/ptaci-chripka-influenzadrubeze/vyskyt-ptaci-chripky-v-evrope-a-ve-svete-2018/ Emergency veterinary measures, which are issued by the Regional Veterinary Administration in the event of an outbreak and which are binding within a defined restricted area around the outbreak (the protection and surveillance zone), also stipulate biosecurity measures for backyard farms in protection zones with the aim preventing the contact of poultry with wild birds and their subsequent possible infection. Increased control (biosecurity) of poultry holdings in contact with avian influenza affected countries was put in place.Additional national emergency veterinary measures to control the spread of HPAI in connection with the second outbreak of HPAI were not applied in Czechia.The general public was informed through the press on compliance with biosecurity in poultry farms, and the current disease situation was published on the website of the State Veterinary Administration: https://www.svscr.cz/zdravi-zvirat/ptaci-chripka-influenza-drubeze/doporuceni-pro-chovatele-drubeze/ Not applied. Not applied. Not applied.The Chief Veterinary Officer in messages about outbreaks reminds poultry farmers about the necessity of following biosecurity principles when handling poultry: https://www.wetgiw.gov.pl/main/grypaptakowIn addition, information on avian influenza is available on the website of the Chief Veterinary Officer (https://www.wetgiw.gov.pl/nadzor-weterynaryjny/grypa-ptakow), including a description of biosecurity rules (https://www.wetgiw.gov.pl/nadzor-weterynaryjny/zasady-ochrony-drobiu-przedgrypa-ptakow). Pursuant to the Regulation of the Minister of Agriculture and Rural Development of 18 December, 2007 on eradication of avian influenza, slaughter / preventive killing of poultry may be implemented in a protection zone, i.e. 3 km around the HPAI outbreak. The competent authority to make a decision on this matter is the District Veterinary Officer. Decisions regarding the slaughter / preventive killing of poultry, related to the occurrence of HPAI in a given protection zone, are taken on the basis of a risk assessment, which takes into account, inter alia, the following areas: the specificity of poultry production in a given district together with the number of commercial / non-commercial farms, possible pathways of the pathogen spread in the environment and potential ways of entering the farm, among others the manner of its protection, as well as topographic conditions of the area, infrastructure and all other circumstances affecting decision taking in the matter in question.In the period covered by the report, preventive culling was carried out on three farms associated with outbreaks 2020/31 and 2020/32. Not applied. Not applied. On 4 April, 2020 the Ministry of the Environment announced a ban on entry to forests from 3 to 11 April, 2020 because of the epidemic of COVID-19, which resulted in no hunting during that period.