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Live-bird markets in the Northeastern United States: a source of avian influenza in commercial poultry
Abstract
Abstract In 1994, an H7N2 subtype avian influenza virus of low pathogenicity was detected in live-bird markets (LBMs) of the Northeast United States. Since that time the H7N2 virus continues to circulate in the ,LBMs despite efforts to eradicate ,the virus by market closures followed by extensive cleaning and disinfection. Since 1996, the LBMs have been implicated as the ,source of virus in five outbreaks of H7N2 avian influenza in commercial poultry. Although the H7N2 virus is of low pathogenicity, several mutations have occurred at, or near, the cleavage site of the haemagglutinin (H) protein, a region of the protein known to influence pathogenicity of H5 and H7 avian influenza viruses. From 1994 to 2002, the amino-acid motif at the H cleavage site has gradually changed from PENPKTR/GLF to PEKPKKR/GLF, with the addition of two lysine (K) residues. Also, a 24-nucleotide deletion, believed to be part of the receptor-bindingregion, was first observed in LBM H7N2 isolates in 1996 and isseen in all isolates tested since 2000. These findings support the need to continue avian influenza virus (AIV) surveillance in the ,LBMs and to develop ,new ,and innovative methods ,to prevent ,the introduction of AIV into the LBMs and to find ways to eliminate it when it is detected. Live-bird markets (LBMs) have been intensely studied in recent ,years because avian influenza viruses in the markets are closely associated with avian influenza in commercial,poultry and ,the markets ,may ,serve as a ,‘fertile ground’ for virus mutations and emergence,of new influenza viruses with increased virulence or ability to infect other species, including humans. In1997, an H5N1 avian influenza virus (AIV) emerged in Hong Kong LBMs to infect 18 people; 6 of whom,died (Claas et al. 1998). The source of human infections was due to direct contact with infected chickens in the LBMs; there was no human-to- human,spread. Subsequent studies on the ,H5N1 virus showed ,that the virus most
... The Northeast (NE) United States (US) has the largest number of LBMs in the USA with a complex system of production flocks, dealers/haulers, and markets (Garber et al. 2007;Jagne, Bennett, and Collins 2021). The LBMs in the NE US, consisting of more than 140 markets across 8 states [Pennsylvania (PA), New York (NY), New Jersey (NJ), Connecticut (CT), Rhode Island (RI), Maryland (MD), Massachusetts (MA), and New Hampshire (NH)], serve as a major source of fresh poultry meat products for mainly ethnic immigrant populations in large cities (Senne, Pedersen, and Panigrahy 2005). Avian influenza surveillance in these markets is voluntary under the 'Prevention and Control of H5 and H7 Avian Influenza in the Live Bird Marketing System Uniform Standards for a State Federal-Industry Cooperative Program (USDA-APHIS 2020)'. ...
... The frequent detections of AIV from LBMs raised public health concerns. The NE US LBMs were identified as the probable source of the virus responsible for the Pennsylvania H5N2 low pathogenic AIVs (LPAIVs) outbreak in the summer of 1983 which subsequently mutated to high pathogenicity (HP) AIV in October 1983 resulting in the HPAIV outbreak in 1983-4 in PA, VA, and MD (Senne, Pedersen, and Panigrahy 2005). During 1996-2006, the H7N2 LPAIVs spread from LBMs of the NE US causing five consecutive outbreaks in commercial poultry despite the efforts to eradicate the virus by market closures followed by extensive cleaning and disinfection (Akey 2003;Davison, Eckroade, and Ziegler 2003;Dunn et al. 2003). ...
... During 1996-2006, the H7N2 LPAIVs spread from LBMs of the NE US causing five consecutive outbreaks in commercial poultry despite the efforts to eradicate the virus by market closures followed by extensive cleaning and disinfection (Akey 2003;Davison, Eckroade, and Ziegler 2003;Dunn et al. 2003). The voluntary LBM surveillance program was established in NE US LBMs to monitor AIVs after the H5N2 virus outbreak in PA during the mid-1980s (Senne, Pedersen, and Panigrahy 2005). The NE US LBMs have been inspected and tested at least once per quarter, including testing of AIV from five to eleven randomly selected birds of each bird type and environmental samples from each market (Jagne, Bennett, and Collins 2021). ...
Live bird market (LBM) surveillance was conducted in the Northeast United States (US) to monitor for the presence of avian influenza viruses (AIV) in domestic poultry and market environments. A total of 384 H2N2 low pathogenicity AIV (LPAIV) isolated from active surveillance efforts in the live bird market system (LBM) of New York, Connecticut, Rhode Island, New Jersey, Pennsylvania, and Maryland during 2013-2019 were included in this analysis. Comparative phylogenetic analysis showed that a wild bird origin H2N2 virus may have been introduced into the LBMs in Pennsylvania and independently evolved since March 2012 followed by spread to LBMs in New York City during late 2012 - early 2013. LBMs in New York state played a key role in maintenance and dissemination of the virus to LBMs in the Northeast US including reverse spread to Pennsylvania LBMs. The frequent detections in the domestic ducks and market environment with viral transmissions between birds and environment possibly led to viral adaptation and circulation in domestic gallinaceous poultry in LBMs, suggesting significant roles of domestic ducks and contaminated LBM environment as reservoirs in maintenance and dissemination of H2N2 LPAIV.
... There is also similarity in the way poultry flows from production sites all over the Northeast, the Mid-West, Mid-Atlantic and Canada into the urban markets. 3 The poultry value chain for the LBMS in the Northeast is very simple compared to what has been observed in other countries. Poultry are raised on special production farms or commercial farms (spent layers) that sell wholesale to dealers and haulers who in turn sell to LBM owners who sell retail to consumers. ...
... Farms are not allowed to mix poultry species in one location, especially ducks and geese that are known to be natural reservoirs of AIV. 3 Other biosecurity measures include housing birds properly to prevent birds being exposed to migratory waterfowl. Regulations also include training of farm personnel in biosecurity. ...
... The strain was found to be similar to a low pathogenic strain that had been circulating in NY LBMs. 3 Low pathogenic strains of avian influenza (LPAI) were not part of the minimal surveillance programs in place in the 1980s. Despite interventions in closing, cleaning, and disinfecting the markets, LPAIs were responsible for five outbreaks seen on commercial poultry farms from 1996-2002. ...
The live bird marketing system (LBMS) in the Northeastern United States (US) consists of a complex system of production flocks, dealers/haulers and live bird markets (LBMs). The States of New York (NY), Pennsylvania (PA) and New Jersey (NJ) have the most active systems with New York State having the most markets presently at 87. The states of Massachusetts, Maine and Connecticut have very few markets. Live bird markets serve mainly ethnic immigrant populations in large urban centers of Northeastern states. The markets are important in the epidemiology of avian influenza viruses (AIV) especially H5 and H7 strains that have zoonotic potential and an effect on trade with United States trading partners. Massive surveillance efforts are carried out to detect and control the spread of these virus strains in the markets under a state/federal/industry program. The program, named the "Prevention and Control of H5 and H7 Avian Influenza in the Live Bird Marketing System: Uniform Standards for a State-Federal-Industry Cooperative Program" is managed mainly by the states, with the federal government assisting in the lab detection and characterization of viruses isolated from the markets. This paper will describe the Northeastern market systems with emphasis on the largest system in NY State and will give a glimpse into its structure, clientele, general regulations, risk factors and avian influenza surveillance.
... Again he also stated that live birds selling create freshness in the minds of some consumers, but the conditions of typical storefront slaughter facilities are unhygienic and severely compromise the animals' well-being. Again, chickens, ducks, geese, quail, and other birds are confined into restrictive multistage cages and the distressed birds defecating on those below birds (Senne et al., 2003; Kingsbury, 2004 and Fielding et al., 2005) and feathers, feces, as well as, blood and intestines soiled and contaminate the market which help in spreading the virus into the markets (Parry, 2003 and Fong, 2004). Besides, birds that remain unsold at the end of the day may go back to nearby farms, taking whatever new viruses they picked up with them (Appenzeller, 2005). ...
... New York has more live markets than all other states in the Northeast combined. By 2001, inspectors could find the virus at 60 percent of markets at any one time (Mullaney, 2003 and Senne et al., 2003). As the states were failing to control the problem and the virus may have needed only one additional mutation before becoming highly pathogenic, the USDA interceded in 2002, coordinating a system-wide closure of all retail live poultry markets throughout the northeastern United States. ...
... Regardless, despite best efforts at eradication and control, it seems clear that live poultry markets represent a public health risk. USDA researchers concluded that " the rampant reassortment of AIVs (avian influenza viruses) in the LBMs could increase the risk of species crossover because it would increase the chances of the occurrence of the correct constellation of genes to create a virus that replicates efficiently in mammals (Senne et al., 2003 and Suarez et al., 1999). ...
... Many birds produced for food in developing countries are marketed live to consumers, and many ethnic groups and immigrant communities in developed countries also prefer to purchase their poultry live or freshly slaughtered (Senne et al., 2003). Villages and small community markets selling live birds frequently consist of a gathering of native chickens and other species that satisfy the local taste and that are held in cages, in baskets, or tied up for sale. ...
... Although AIV was not monitored for many of the intervening years, it is thought to have been endemic in this LBM system for at least the last decade (Senne et al., 2006) and probably much longer. Poultry sold in the East Coast LBM are supplied not only by nearby farms, which raise birds for sale, but also by backyard flocks and commercial farms, with birds sometimes coming from as far away as Ohio (Senne et al., 2003). The LBM in the Northeast are supplied directly by the producer, but many also acquire poultry through wholesalers or dealers, which are frequently secondary and tertiary sources (Bulaga et al., 2003b;Mullaney, 2003). ...
... The birds from dealers, auction markets, and wholesalers are from many different farms and are housed togeth-er with other avian species and mammals, sometimes overnight, before being delivered to the LBM (Bulaga et al., 2003a). More than 120 markets can be found in 6 states in the Northeast of the United States, most of which are located in New York and New Jersey (Bulaga et al., 2003b;Senne et al., 2003), with a wide range of additional buyers of poultry, including businesses (e.g., restaurants) and the general public. Several attempts have been made to eradicate AIV from the LBM system in the Northeast; however, these attempts have failed and AIV in this LBM system remain endemic (Trock et al., 2008). ...
Live bird markets (LBM) are essential for marketing poultry in many developing countries, and they are a preferred place for
many people to purchase poultry for consumption throughout the world. Live bird markets are typically urban and have a permanent
structure in which birds can be housed until they are sold. Live bird markets bring together a mixture of bird species that
meet the preferences of their customers and that are commonly produced by multiple suppliers. The mixture of species, the
lack of all-in–all-out management, and multiple suppliers are all features that make LBM potential sources of avian influenza
viruses (AIV), especially for their supply flocks. Live bird markets have been linked to many outbreaks of avian influenza
internationally and in the United States. Avian influenza virus is endemic in many, but not all, LBM systems. For instance,
AIV has not been isolated from the Southern California LBM system since December 2005, although the risk of new introductions
remains. The California LBM system is much smaller than the New York system, handles fewer birds, and has fewer bird suppliers,
which, combined with recent avian influenza prevention and control plans, have enabled it to be AIV free for nearly 3 yr.
... These markets house birds from many different sources and species, including waterfowl; they continuously maintain live birds on the premises and, in some cases, may practice suboptimal sanitation. Since 1996, five outbreaks of low pathogenicity H7N2 in commercial poultry have been linked to the LBMS in the northeastern United States (Senne et al. 2003). Of four LPAI outbreaks in Pennsylvania since 1983, two were traced to connections with live-bird markets (Dunn et al. 2003). ...
... Since 1987, extensive surveillance has been conducted in the LBMS to identify circulating viruses. Surveillance activities were reviewed in 2003 (Senne et al. 2003)Live-bird market surveillance has demonstrated that it is capable of detecting H5/H7 viruses, but not how likely it is to detect every outbreak. The data suggest that markets tested only once per year rarely reveal infection, while those tested multiple times frequently detect viruses. ...
... Intensive cleaning and disinfection of all markets was accomplished during a 3-day, poultry-free closure period. This coordinated market closure resulted in a drastic reduction in the presence of LPAI [10]. This success led to changes in coordinated efforts by participating states in monitoring and testing for avian influenza. ...
Avian influenza in domestic poultry can have varied impacts on the health and welfare of birds and an economic burden on producers, consumers, and animal health agencies including the cost to control and eradicate avian influenza. Low pathogenic avian influenza has historically been a recurring issue in U.S. live bird markets, but rarely studied. Live bird markets source various species of birds and mammals from a variety of wholesalers and sell either live animals or freshly harvested animals. Using cost estimates from the 2016 outbreak of low pathogenic avian influenza in northeastern U.S. live bird markets, estimates of the mean per market costs were calculated for responding government agencies ($804) and the market itself ($3,997), including traceback investigation, testing costs, and cleaning and disinfection. The economic impact also included market impacts which the majority are affected by income that the live bird markets forego during cleaning and disinfection ($3,998 per market) with an expected shutdown of 3–5d. Animal health agencies' responses to a disease depend on the established disease response and resources, such as labor and funding. Understanding the economic costs of disease management improves the decision-making process for these agencies and markets as a whole to limit disease introduction, spread, longevity, and market impacts through business disruptions and foregone income.
... For example, a low pathogenic (LP) AIV was detected in multiple LBMs in southern California during 2005 [5], and a highly pathogenic (HP) AIV has been detected in LBMs in Asia and Africa [1,19]. In some instances, the conditions found in these types of markets are ideal for establishment and transmission of AIVs [19] and LBMs have been suggested as the viral source of previous outbreaks in commercial poultry in the northeastern U.S. [14]. Notably, LP H5 AIVs have been detected in LBMs in the northeastern U.S. as recently as the summer of 2016 [11]. ...
Abstract Live bird markets are common in certain regions of the U.S. and in other regions of the world. We experimentally tested the ability of a wild bird influenza A virus to transmit from index animals to naı¨ve animals at varying animal densities in stacked cages in a simulated live bird market. Two and six mallards, five and twelve quail, and six and nine pheasants were used in the low-density and high-density stacks of cages, respectively. Transmission did not occur in the high-density stack of cages likely due to the short duration and relatively low levels of shedding, a dominance of oral shedding, and the lack of transmission to other mallards in the index cage. In the low-density stack of cages, transmission occurred among all species tested, but not among all birds present. Oral and cloacal shedding was detected in waterfowl but only oral shedding was identified in the gallinaceous birds tested. Overall, transmission was patchy among the stacked cages, thereby
suggesting that chance was involved in the deposition of shed virus in key locations (e.g., food or water bowls),
which facilitated transmission to some birds.
... Most of the poultry kept in developing countries is sold to consumers from LBMs either in live or freshly slaughtered form (Senne et al., 2003). However, handling of poultry in LBMs has previously been associated with increase of exposure to AI viruses (Van Kerkhove et al., 2011) in outbreak countries. ...
Live bird markets (LBMs) are essential for marketing poultry, but have been linked to many outbreaks of avian influenza (AI) and its spread. In Uganda, it has been observed that demographic characteristics of poultry traders/handlers influence activities and decision-making in LBMs. The study investigated the influence of socio-demographic characteristics of poultry handlers: age, sex, religion, educational background, level of income, location of residence and region of operation on 20 potential risk factors for introduction and spread of AI in LBMs. Study sites included 39 LBMs in the four regions of Uganda. Data was collected using a semi-structured questionnaire administered to 424 poultry handlers. We observed that background of education was a predictor for slaughter and processing of poultry in open sites. Location of residence was associated with slaughter of poultry from open sites and selling of other livestock species. Region influenced stacking of cages, inadequate cleaning of cages, feeders and drinkers, and provision of dirty feed and water. Specifically, bird handlers with secondary level of education (OR = 12.9, 95% CI: 2.88–57.4, P < 0.01) were more likely to be involved in open site slaughter of poultry than their counterparts without formal education. Comparatively, urbanite bird handlers were less likely to share poultry equipment (OR = 0.4, 95% CI: 0.22–0.63, P < 0.01) than rural resident handlers. Poultry handlers in Northern were 3.5 times more likely to practise insufficient cleaning of cages (OR = 3.5, 95% CI: 1.52–8.09) compared to those in Central region. We demonstrated that some socio-demographic characteristics of poultry handlers were predictors to risky practices for introduction and spread of AI viruses in LBMs in Uganda.
... guinea fowl; Numida meleagris), among others (Swayne, 2008). Collectively, not only can these species be found in the wild, but they are also normally raised in outdoor operations, which have higher AIV infection rates than intensive industrial poultry (Shortridge, 1999), or are found in live poultry market systems (Senne et al., 2005). Therefore, minor avian species could be considered bridge species in the poultry–wildlife interface, which highlights their interest from the transmission and biosecurity points of view. ...
Susceptibility to avian influenza viruses (AIVs) can vary greatly among bird species. Chickens and turkeys are major avian species that, like ducks, have been extensively studied for avian influenza. To a lesser extent, minor avian species such as quail, partridges, and pheasants have also been investigated for avian influenza. Usually, such game fowl species are highly susceptible to highly pathogenic AIVs and may consistently spread both highly pathogenic AIVs and low-pathogenic AIVs. These findings, together with the fact that game birds are considered bridge species in the poultry-wildlife interface, highlight their interest from the transmission and biosecurity points of view. Here, the general pathobiological features of low-pathogenic AIV and highly pathogenic AIV infections in this group of avian species have been covered.
... Spillover from wild waterfowl has been implicated in outbreaks of AIV in domestic poultry[31,54,55,56]. In the United States this has been of particular concern in the Great Lakes region where the turkey industry has experienced production losses resulting from AIV[31,55,57]and in the New England region where the live bird marketing system has repeatedly experienced outbreaks of AIV[58,59,60]. Furthermore the presence of AIV in wild waterfowl has been linked to increased transmission efficiency among sympatric populations of domestic poultry[61]. ...
Outbreaks of avian influenza in North American poultry have been linked to wild waterfowl. A first step towards understanding where and when avian influenza viruses might emerge from North American waterfowl is to identify environmental and demographic determinants of infection in their populations. Laboratory studies indicate water temperature as one determinant of environmental viral persistence and we explored this hypothesis at the landscape scale. We also hypothesized that the interval apparent prevalence in ducks within a local watershed during the overwintering season would influence infection probabilities during the following breeding season within the same local watershed. Using avian influenza virus surveillance data collected from 19,965 wild waterfowl across the contiguous United States between October 2006 and September 2009 We fit Logistic regression models relating the infection status of individual birds sampled on their breeding grounds to demographic characteristics, temperature, and interval apparent prevalence during the preceding overwintering season at the local watershed scale. We found strong support for sex, age, and species differences in the probability an individual duck tested positive for avian influenza virus. In addition, we found that for every seven days the local minimum temperature fell below zero, the chance an individual would test positive for avian influenza virus increased by 5.9 percent. We also found a twelve percent increase in the chance an individual would test positive during the breeding season for every ten percent increase in the interval apparent prevalence during the prior overwintering season. These results suggest that viral deposition in water and sub-freezing temperatures during the overwintering season may act as determinants of individual level infection risk during the subsequent breeding season. Our findings have implications for future surveillance activities in waterfowl and domestic poultry populations. Further study is needed to identify how these drivers might interact with other host-specific infection determinants, such as species phylogeny, immunological status, and behavioral characteristics.
... Pandemic concerns aside, HPAI outbreaks have potential social (Cristalli and Capua 2007), economic (Clague et al. 2006), occupational (Swayne 2006), agricultural (Spala et al. 2006), trade (Domenech et al. 2006), public health (Beigel et al. 2005), veterinary (Capua and Alexander 2006b), animal conservation (Roberton et al. 2006), and welfare (Serratosa et al. 2007) implications. When an LPAI H5 or H7 virus from the aquatic bird reservoir is introduced into a population of terrestrial poultry either through a live bird market interaction (Senne et al. 2003) or similar biosecurity breach (Capua and Marangon 2000), the LPAI virus may, within weeks (Rojas et al. 2002) or months (Naeem et al. 2007), unpredictably mutate into an HPAI virus (Capua and Marangon 2003b). By their nature, LPAI viruses may be difficult to detect, but, in a few cases, the avirulent progenitors of HPAI outbreaks have been identified before the transformation, as with outbreaks in Pennsylvania starting in 1983 (Kawaoka and Webster 1985), Mexico in 1994 (Horimoto et al. 1995), Italy in 1999 (), Chile in 2002 (Suarez et al. 2004), Pakistan in 2003 (Naeem et al. 2007), and Canada in 2004 (Power 2005), offering opportunities to study both the genetic changes that take place and risk factors for emergence. ...
Emerging infectious diseases, most of which are considered zoonotic in origin, continue to exact a significant toll on society. The origins of major human infectious diseases are reviewed and the factors underlying disease emergence explored. Anthropogenic changes, largely in land use and agriculture, are implicated in the apparent increased frequency of emergence and re-emergence of zoonoses in recent decades. Special emphasis is placed on the pathogen with likely the greatest zoonotic potential, influenza virus A.
Avian influenza viruses (AIVs) continue to impose a negative impact on animal and human health worldwide. In particular, the emergence of highly pathogenic AIV H5 and, more recently, the emergence of low pathogenic AIV H7N9 has led to enormous socio-economical losses in the poultry industry and resulted in fatal human infections. While H5N1 remains infamous, the number of zoonotic infections with H7N9 has far surpassed those attributed to H5. Despite the clear public health concerns posed by AIV H7, it is unclear why specifically this virus became endemic in poultry and emerged in humans. In this review, we bring together data on global patterns of H7 circulation, evolution, and emergence in humans. Specifically, we discuss data from the wild bird reservoir, expansion and epidemiology in poultry, the significant increase of their zoonotic potential since 2013, and genesis of highly pathogenic H7. In addition, we analysed available sequence data from an evolutionary perspective, demonstrating patterns of introductions into distinct geographic regions and reassortment dynamics. The integration of all aspects is crucial in the optimisation of surveillance efforts in wild birds, poultry and humans, and we emphasize the need for a One Health approach in controlling emerging viruses such as H7 AIV.
An outbreak of influenza A(H7N2) virus in cats in a shelter in New York, NY, USA, resulted in zoonotic transmission. Virus isolated from the infected human was closely related to virus isolated from a cat; both were related to low pathogenicity avian influenza A(H7N2) viruses detected in the United States during the early 2000s. © 2017, Centers for Disease Control and Prevention (CDC). All rights reserved.
In 2014 and 2015, the United States experienced an unprecedented outbreak of Eurasian clade 2.3.4.4 H5 highly pathogenic avian influenza (HPAI) virus. Initial cases affected mainly wild birds and mixed backyard poultry species, while later outbreaks affected mostly commercial chickens and turkeys. The pathogenesis, transmission, and intrahost evolutionary dynamics of initial Eurasian H5N8 and reassortant H5N2 clade 2.3.4.4 HPAI viruses in the United States were investigated in minor gallinaceous poultry species (i.e., species for which the U.S. commercial industries are small), namely, Japanese quail, bobwhite quail, pearl guinea fowl, chukar partridges, and ring-necked pheasants. Low mean bird infectious doses (<2 to 3.7 log10) support direct introduction and infection of these species as observed in mixed backyard poultry during the early outbreaks. Pathobiological features and systemic virus replication in all species tested were consistent with HPAI virus infection. Sustained virus shedding with transmission to contact-exposed birds, alongside long incubation periods, may enable unrecognized dissemination and adaptation to other gallinaceous species, such as chickens and turkeys. Genome sequencing of excreted viruses revealed numerous low-frequency polymorphisms and 20 consensus-level substitutions in all genes and species, but especially in Japanese quail and pearl guinea fowl and in internal proteins PB1 and PB2. This genomic flexibility after only one passage indicates that influenza viruses can continue to evolve in galliform species, increasing their opportunity to adapt to other species. Our findings suggest that these gallinaceous poultry are permissive for infection and sustainable transmissibility with the 2014 initial wild bird-adapted clade 2.3.4.4 virus, with potential acquisition of mutations leading to host range adaptation.
Avian influenza virus (AIV) is a global virus that knows no geographic boundaries, has no political agenda, and can infect poultry irrespective of their occupying ecosystem, agricultural production system, or other anthropocentric niches. AIVs or evidence of their infection have been detected in poultry and wild birds on all seven continents, but the largest numbers of cases detected have been in North America and Europe, where intensive surveillance is conducted in poultry and wild birds. Since 1959, there have been 37 epizootics of highly pathogenic avian influenza in poultry and wild birds, the largest one being the H5N1 HPAI epizootic, which began in China in 1996 and continues today. This epizootic has involved 67 countries in Asia, Africa, Europe, and North America, and has affected more than 400 million birds.
Over thousands of years, human activity has changed the natural ecosystems of birds by domestication, and their influenza A viruses (IAVs) have reassorted and adapted to new systems and hosts. At high risk for introduction of IAVs from free-living aquatic birds are outdoor-reared domestic poultry, especially domestic waterfowl (ducks and geese). Today, diverse IAVs cause sporadic infections in a variety of wild and domestic mammals and poultry, and a limited number of IAVs cause endemic respiratory disease in horses, pigs, humans, and domestic poultry. HPAIVs have arisen by mutation of H5 and H7 LPAIVs, usually following uncontrolled circulation of the viruses in susceptible gallinaceous poultry.
The World Organization for Animal Health provides sanitary standards for international trade, and emphasizes science-based risk assessment for safe trade of animals and animal products. The goal is to prevent unacceptable risks to animal and human health while avoiding unjustified or politically motivated trade barriers. The spread of animal influenza virus (AIV) is greatest through trade of infected animals and to a lesser extent trade of their products. Specifically, the risk of importation of swine or low-pathogenic avian influenza viruses through meat is negligible, as these viruses are not present in meat, but high-pathogenicity avian influenza virus can be present in poultry meat and eggs, making the importation of such commodities from affected countries an unacceptable risk, unless the risk is mitigated by vaccination of poultry or by using inactivation processes such as cooking or pasteurization of product. AIV is primarily an animal health issue rather than a human health or food safety issue.
This chapter reviews the direct and indirect control measures for influenza infections in animals: poultry, swine, dogs, and horses. Regulations and guidelines linked to the international movements of animals for trade or other purposes are also addressed, as well as statutory requirements whenever applicable.
Highly pathogenic avian influenza viruses of the H5N1 subtype emerged in Far East Asia in 1996 and spread in three continents in a period of 10 or less years. Before this event, avian influenza infections caused by highly pathogenic viruses had occurred in many different countries, causing minor or major outbreaks, and had always been eradicated. The unique features of these H5N1 viruses combined to the geographic characteristics of the area of emergence, including animal husbandry practices, has caused this subtype to become endemic in several Asian countries, as well as in Egypt. Our aim is to review the direct and indirect control strategies with the rationale for use, advantages and shortcomings - particularly resulting from practicalities linked to field application and economic constraints. Certainly, in low income countries which have applied vaccination, this has resulted in a failure to eradicate the infection. Although the number of infected countries has dropped from over 40 (2006) to under 10 (2012), the extensive circulation of H5N1 in areas with high poultry density still represents a risk for public and animal health.
The emergence of highly pathogenic avian influenza (HPAI) of Asian lineage and the subsequent spillover to other part of the globe and on going spread of Eurasian-Africa H5N1 epidemic into domestic, wild birds and human have generated unprecedented attention in recent times and threat of potential pandemic via the avian-human link. Historically, from 1878 through 1955, fowl plaque was described as a high mortality disease of poultry in many countries throughout Europe, Asia, North and South America and Africa and the etiology was proved to be a filterable virus. In the 1930s through the 1950s, fowl plaque disappeared as an endemic disease in most part of the world. In 1949, the first report of a low virulent disease in chickens caused by LPAI virus was reported. In 1955, the etiological of fowl plaque was determined to be influenza A virus, which subsequently was identified as the H7 subtype. In 1959, a "fowl plaque-like" outbreak was described in chickens, which was the first report of fowl plaque caused by a non-H7 AI virus, i.e. first fowl plaque outbreak from H5 subtype of AI virus. In 1961 the first wild birds infection and deaths were reported in common terns of South Africa. In 1966 and 1971, the first H5 and H7 LPAI viruses, respectively were identified; prior to this period, only HPAI viruses had H5 and H7 subtypes. In 1970, the AGID serological test was introduced, which allowed easy and rapid identification of AI virus-infected poultry flocks. In 1972, there was the first isolation of LPAI viruses in asymptomatic wild birds: ducks in the United State and shorebirds in Australia. In 1981, the term "highly pathogenic avian influenza" was accepted as standard nomenclature for fowl plaque and related synonyms. In 1983, LPAI virus was observed mutating to HPAI virus during LPAI field outbreak, and specific genomic changes were identified in the proteolytic cleavage site of the hemagglutinin responsible for the virulence change. In the late 1980s and early 1990s, molecular criteria were added to the definition for classifying an AI virus as HPAI. In 2002, there were the first reported infections and deaths in a wide variety of wild bird species from AI virus H5N1 HPAI virus. The primary goal of this review is to highlight the global situation of HPAI and provide baseline information to show the potential pandemic nature of the virus, so that control and prevention strategies can be improved.
Global Production and Trade of Poultry Transmission Risk through Trade Mitigation of Trade Risks Food Safety Risks Conclusions? References
Oropharyngeal and cloacal swabs were collected from poultry sold in two live bird market (LBM) systems to estimate the prevalence of low pathogenicity avian influenza virus (LPAIV) shedding during the summer and fall of 2005. Random sampling was conducted in three LBMs in Minnesota where 50 birds were sampled twice weekly for 4 wk, and in three LBMs in a California marketing system. A stratified systematic sampling method was used to collect samples from Southern California LBMs, where LPAIV was detected during routine surveillance. No LPAIV was detected in the LBM system in Minnesota where realtime reverse transcription-PCR (RT-PCR) was conducted on oropharyngeal samples. RT-PCR was performed on swabs taken from 290 of 14,000, 65 of 252, and 60 of 211 birds at the three Southern California LBMs. The number of samples collected was based on the number of birds, age of the birds, and number of species present in the LBM. Virus isolation, subtyping, and sequencing of the hemagglutinin, neuraminidase, and other internal protein genes was performed on AIV-positive samples. The estimated prevalence of LPAIV in California was 0.345% in an LBM/supply farm with multiple ages of Japanese quail, 3% in an LBM with multiple ages and strains of chickens present, and 49.8% in an LBM with multiple species, multiple strains, and multiple ages. The positive virus samples were all LPAIV H6N2 and closely related to viruses isolated from Southern California in 2001 and 2004. Little or no comingling of poultry may contribute to little or no LPAIV detection in the LBMs.
Although live bird markets (LBMs) have been associated with outbreaks of avian influenza (AI), there are some LBM systems where AI outbreaks are extremely rare events. The California LBMs have not had any detected avian influenza viruses (AIVs) since December 2005. Responses to a detailed questionnaire on the practices and characteristics of the participants in the California low-pathogenic (LP) AI control program have been described to characterize possible reasons for the lack of AI outbreaks in LBMs. Compliance with an LPAI control program that contains active surveillance, prevention, and rapid response measures by those involved in the LBM system, rendering services to dispose of carcasses, no wholesalers, and few third-party bird deliveries was associated with the lack of LPAIV circulating in the Southern California LBM system.
Jack Gelb The pathogenicity of twelve recent low-pathogenicity H7 avian influenza isolates was evaluated through clinical signs, relative oral/pharyngeal (O/P) and cloacal viral shed, serology, histopathology and immunohistochemistry in SPF leghorns, Pekin ducks, and turkeys. Gene constellation and phylogenetic analysis revealed that seven of the isolates (CK/MD/MinMah/04, TK/VA/67/02, GH/MA/1408081-11/02, CK/PA/9801289/98, CK/NY/3112-1/95, TK/NY/4550-5/94, and CK/NY/30749-3/00) were typical of the low-pathogenicity H7N2 lineage viruses circulating in live bird markets while five isolates (Pintail/MN/423/99, Mallard/OH/421/87, Ruddy Turnstone/DE/1538/00, CK/NJ/15086-3/94, and CK/NY/12273-11/99) were found to be of wild-bird origin. Four pathogenicity trials were conducted to evaluate these twelve isolates that had been characterized (Southeast Poultry Research Laboratory) as low-pathogenicity avian influenza. Phylogenetic analysis of the HA1 sequence revealed multiple sublineages in the H7 subtype, four of the sublineages are represented in this study to determine differences in pathogenesis. University of Delaware, Department of Animal and Food Sciences M.S.
The virulence of low pathogenicity (LP) type A H7N2 avian influenza virus (AIV) isolates recovered from chickens in Delaware and the eastern shore of Maryland in 2004 was evaluated. Three-week-old leghorn- and broiler-type chickens and turkeys were inoculated via the conjunctival sac with 10(3.5)-10(4.0) 50% embryo infections dose (EID50) of virus per bird with A/ chicken/Delaware/Viva/04, A/chicken/Delaware/Hobo/04, and A/chicken/Maryland/Minh Ma/04. In broilers, the viruses produced respiratory signs, airsacculitis, and microscopic lesions in the trachea and lung. In contrast, signs and lesions were less severe in turkeys, and they were rarely observed in specific-pathogen-free (SPF) leghorns. In broilers and SPF leghorns, AIV peaked on day 3 postinoculation (PI), based on virus isolation and real-time reverse transcription-polymerase chain reaction, and antigen capture testing. Infection in turkeys peaked on day 7 PI. Serum antibodies generally were detected earlier in broilers (day 7 PI) than in turkeys or SPF leghorns (day 14 PI) using agar gel immunodiffusion, hemagglutination-inhibition, and the enzyme-linked immunosorbent assay. A second trial was performed to further examine the disease susceptibility of the leghorn chicken given the comparatively mild responses noted in the first trial. A 10-fold higher dose of 10(4.5)-10(5.0)EID50 per chick given via the conjunctival sac was used. In addition, commercial-type leghorns were tested as were chicks from the SPF leghorn source. The higher AIV dose resulted in more rapid and consistent rates of infection and higher serum antibody responses in both types of leghorn chickens. However, as observed in the first trial, clinical signs and microscopic lesions in both types of leghorns were infrequent and very mild. These findings indicate leghorn-type chickens, which are commonly used for pathogenicity assessments because of their availability, may not be the most suitable host for evaluating the virulence potential of LP AIV.
The mean infectious doses of selected avian influenza virus (AIV) isolates, determined in domestic poultry under experimental conditions, were shown to be both host-dependent and virus strain-dependent and could be considered one measure of the infectivity and adaptation to a specific host. As such, the mean infectious dose could serve as a quantitative predictor for which strains of AIV, given the right conditions, would be more likely transmitted to and maintained in a given species or subsequently cause an AI outbreak in the given species. The intranasal (IN) mean bird infectious doses (BID50) were determined for 11 high-pathogenicity AIV (HPAIV) isolates of turkey and chicken origin for white leghorn (WL) chickens, and for low-pathogenicity AIV (LPAIV) isolates of chicken (n = 1) and wild mallards (n = 2) for turkeys, and WL and white Plymouth rock (WPR) chickens, domestic ducks and geese, and Japanese quail. The BID50 for HPAIV isolates for WL chickens ranged from 10(1.2) to 10(4.7) mean embryo infectious dose (EID50) (median = 10(2.9)). For chicken-origin HPAIV isolates, the BID50 in WL chickens ranged from 10(1.2) to 10(3.0) EID50 (median = 10(2.6)), whereas for HPAIV isolates of turkey origin, the BID50 in WL chickens was higher, ranging from 10(2.8) to 10(4.7) EID50 (median = 10(3.9)). The BID50 of 10(4.7) was for a turkey-origin HPAIV virus that was not transmitted to chickens on the same farm, suggesting that, under the specific conditions present on that farm, there was insufficient infectivity, adaptation, or exposure to that virus population for sustained chicken transmission. Although the upper BID50 limit for predicting infectivity and sustainable transmissibility for a specific species is unknown, a BID50 < 10(4.7) was suggestive of such transmissibility. For the LPAIVs, there was a trend for domestic ducks and geese and Japanese quail to have the greatest susceptible and for WL chickens to be the most resistant, but turkeys were susceptible to two LPAIV tested when used at moderate challenge doses. This suggests domestic ducks and geese, turkeys, and Japanese quail could serve as bridging species for LPAIVs from wild waterfowl to chickens and other gallinaceous poultry. These data do provide support for the commonly held and intuitive belief that mixing of poultry species during rearing and in outdoor production systems is a major risk factor for interspecies transmission of AIVs and for the emergence of new AIV strains capable of causing AI outbreaks because these situations present a more diverse host population to circumvent the natural host dependency or host range of circulating viruses.
In 1997, an H5N1 influenza virus outbreak occurred in chickens in Hong Kong, and the virus was transmitted directly to humans. Because there is limited information about the avian influenza virus reservoir in that region, we genetically characterized virus strains isolated in Hong Kong during the 1997 outbreak. We sequenced the gene segments of a heterogeneous group of viruses of seven different serotypes (H3N8, H4N8, H6N1, H6N9, H11N1, H11N9, and H11N8) isolated from various bird species. The phylogenetic relationships divided these viruses into several subgroups. An H6N1 virus isolated from teal (A/teal/Hong Kong/W312/97 [H6N1]) showed very high (>98%) nucleotide homology to the human influenza virus A/Hong Kong/156/97 (H5N1) in the six internal genes. The N1 neuraminidase sequence showed 97% nucleotide homology to that of the human H5N1 virus, and the N1 protein of both viruses had the same 19-amino-acid deletion in the stalk region. The deduced hemagglutinin amino acid sequence of the H6N1 virus was most similar to that of A/shearwater/Australia/1/72 (H6N5). The H6N1 virus is the first known isolate with seven H5N1-like segments and may have been the donor of the neuraminidase and the internal genes of the H5N1 viruses. The high homology between the internal genes of H9N2, H6N1, and the H5N1 isolates indicates that these subtypes are able to exchange their internal genes and are therefore a potential source of new pathogenic influenza virus strains. Our analysis suggests that surveillance for influenza A viruses should be conducted for wild aquatic birds as well as for poultry, pigs, and humans and that H6 isolates should be further characterized.
Outbreaks of avian influenza due to an H7N1 virus of low pathogenicity occurred in domestic poultry in northern Italy from March 1999 until December 1999 when a highly pathogenic avian influenza (HPAI) virus emerged. Nucleotide sequences were determined for the HA1 and the stalk region of the neuraminidase (NA) for viruses from the outbreaks. The HPAI viruses have an unusual multibasic haemagglutinin (HA) cleavage site motif, PEIPKGSRVRRGLF. Phylogenetic analysis showed that the HPAI viruses arose from low pathogenicity viruses and that they are most closely related to a wild bird isolate, A/teal/Taiwan/98. Additional glycosylation sites were present at amino acid position 149 of the HA for two separate lineages, and at position 123 for all HPAI and some low pathogenicity viruses. Other viruses had no additional glycosylation sites. All viruses examined from the Italian outbreaks had a 22 amino acid deletion in the NA stalk that is not present in the N1 genes of the wild bird viruses examined. We conclude that the Italian HPAI viruses arose from low pathogenicity strains, and that a deletion in the NA stalk followed by the acquisition of additional glycosylation near the receptor binding site of HA1 may be an adaptation of H7 viruses to a new host species i.e. domestic poultry.
An outbreak of low-pathogenicity H7N2 avian influenza virus (AIV) in the Shenandoah Valley of Virginia during the spring and summer of 2002 affected 197 farms and resulted in the destruction of over 4.7 million birds. The outbreak affected primarily turkey farms (28 breeders, 125 grow out) with some spillover into chicken farms (29 breeders, 13 grow out, 2 table-egg layers). Although no direct link was established, the strain of H7N2 AIV in this outbreak had a molecular fingerprint that was essentially identical to the H7N2 AIV strain that has circulated in the live bird markets of the northeastern United States for the last 8 yr. After an initial delay caused by lack of viable disposal options, depopulation and disposal, primarily in sanitary landfills, was carried out within 24 hr of detection of a positive flock. Increased surveillance efforts included once-a-week testing of the daily mortality of all poultry farms in the region, testing of all breeder farms every 2 wk, and testing of all flocks prior to movement for any reason. A statistical sampling of backyard flocks and wild birds found no evidence of the virus. The successful eradication of this outbreak was the result of the efforts of a highly effective task force of industry state, and federal personnel.
The A/Chick/Penn/83 (H5N2) influenza virus that appeared in chickens in Pennsylvania in April 1983 and subsequently became virulent in October 1983, was examined for plaque-forming ability and cleavability of the hemagglutinin (HA) molecule. The avirulent virus produced plaques and cleaved the HA only in the presence of trypsin. In contrast, the virulent virus produced plaques and cleaved the HA precursor into HA1 and HA2 in the presence or absence of trypsin. The apparent molecular weight of the HA1 from the avirulent virus was higher than that from the virulent virus, but when the viruses were grown in the presence of tunicamycin, the molecular weights of HA were indistinguishable. Two of nine monoclonal antibodies to the HA of the avirulent virus indicate that there is at least one epitope on the HA that is different between the virulent and avirulent viruses. The amino acid sequences of the HAs from the two viruses were compared by sequencing their respective HA gene. The nucleotide sequence coding for the processed HA polypeptide contained 1641 nucleotides specifying a protein of 547 amino acids. The amino acid sequences of the virulent and avirulent viruses were indistinguishable through the connecting peptide region, indicating that the difference in cleavability of the H5 HA is not directly attributed to the amino acid sequence of the connecting peptide. Four of seven nucleotide changes resulted in amino acid changes at residues 13, 69, and 123 of HA1 and at residue 501 of the HA2 polypeptide. Since there were no deletions or insertions in the amino acid sequence of the virulent or avirulent viruses, the possibility exists that the difference in molecular weight is due to loss of a carbohydrate side chain in the virulent strain. The amino acid change in the virulent strain at residue 13 is the only mutation that could affect a glycosylation site and this is in the vicinity of the connecting peptide. It is postulated that the loss of this carbohydrate may permit access of an enzyme that recognizes the basic amino acid sequences and results in cleavage activation of the HA in the virulent virus.
In October of 1993, there was decreased egg production and increased mortality among Mexican chickens, in association with serologic evidence of an H5N2 influenza virus. First isolated from chickens in May of 1994, after spreading widely in the country, the virus caused only a mild respiratory syndrome in specific pathogen-free chickens. Because eradication of the virus by destruction of infected birds posed major obstacles to the poultry industry in Mexico, we were able to conduct a "field experiment" to determine the fate of an avirulent virus after repeated cycles of replication in millions of chickens. By the end of 1994, the virus had mutated to contain a highly cleavable hemagglutinin (HA), but remained only mildly pathogenic in chickens. Within months, however, it had become lethal in poultry. Nucleotide sequence analysis of the HA cleavage site of the original avirulent strain revealed R-E-T-R, typical of avirulent viruses and unlike the K-K-K-R sequence characterizing viruses responsible for the 1983 outbreak in poultry in the United States. Both mildly and highly pathogenic isolates contained insertions and a substitution of basic residues in the HA connecting peptide, R-K-R-K-T-R, which made the HA highly cleavable in trypsin-free chicken embryo fibroblasts. Phylogenetic analysis of the HA of H5 avian influenza viruses, including the Mexican isolates, indicated that the epidemic virus had originated from the introduction of a single virus of the North American lineage into Mexican chickens. This sequence of events demonstrates, apparently for the first time, the stepwise acquisition of virulence by an avian influenza virus in nature.
In May, 1997, a 3-year-old boy in Hong Kong was admitted to the hospital and subsequently died from influenza pneumonia, acute respiratory distress syndrome, Reye's syndrome, multiorgan failure, and disseminated intravascular coagulation. An influenza A H5N1 virus was isolated from a tracheal aspirate of the boy. Preceding this incident, avian influenza outbreaks of high mortality were reported from three chicken farms in Hong Kong, and the virus involved was also found to be of the H5 subtype.
We carried out an antigenic and molecular comparison of the influenza A H5N1 virus isolated from the boy with one of the viruses isolated from outbreaks of avian influenza by haemagglutination-inhibition and neuraminidase-inhibition assays and nucleotide sequence analysis.
Differences were observed in the antigenic reactivities of the viruses by the haemagglutination-inhibition assay. However, nucleotide sequence analysis of all gene segments revealed that the human virus A/Hong Kong/156/97 was genetically closely related to the avian A/chicken/Hong Kong/258/97.
Although direct contact between the sick child and affected chickens has not been established, our results suggest transmission of the virus from infected chickens to the child without another intermediate mammalian host acting as a "mixing vessel". This event illustrates the importance of intensive global influenza surveillance.
The origin of the H5N1 influenza viruses that killed six of eighteen infected humans in 1997 and were highly pathogenic in chickens has not been resolved. These H5N1 viruses transmitted directly to humans from infected poultry. In the poultry markets in Hong Kong, both H5N1 and H9N2 influenza viruses were cocirculating, raising the possibility of genetic reassortment. Here we analyze the antigenic and genetic features of H9N2 influenza viruses with different epidemiological backgrounds. The results suggest that the H9N2 influenza viruses of domestic ducks have become established in the domestic poultry of Asia. Phylogenetic and antigenic analyses of the H9N2 viruses isolated from Hong Kong markets suggest three distinct sublineages. Among the chicken H9N2 viruses, six of the gene segments were apparently derived from an earlier chicken H9N2 virus isolated in China, whereas the PB1 and PB2 genes are closely related to those of the H5N1 viruses and a quail H9N2 virus-A/quail/Hong Kong/G1/97 (Qa/HK/G1/97)-suggesting that many of the 1997 chicken H9 isolates in the markets were reassortants. The similarity of the internal genes of Qa/HK/G1/97 virus to those of the H5N1 influenza viruses suggests that the quail virus may have been the internal gene donor. Our findings indicate that the human and poultry H5N1 influenza viruses in Hong Kong in 1997 were reassortants that obtained internal gene segments from Qa/HK/G1/97. However, we cannot be certain whether the replicate complex of H5N1 originated from Qa/HK/G1/97 or whether the reverse transfer occurred; the available evidence supports the former proposal.
Over the last 10 years, low-pathogenicity avian influenza (LPAI) viruses have been isolated from the live-bird markets (LBMs) of the Northeast. Despite educational efforts, surveillance, and increased state regulatory efforts, the number of positive markets has persisted and increased. In an effort to address the continued levels of LPAI in the retail LBM and address the question of persistence and circulation of the virus within the LBM system itself, these markets were closed for a continuous 3-day period. This effort was a cooperative effort between the State Departments of Agriculture and coordinated by the U.S. Department of Agriculture and led to the first successful system-wide closure of the retail LBMs in the Northeast.
The nonpathogenic avian influenza (AI) outbreak in Pennsylvania began in December 1996 when there was a trace back from a New York live bird market to a dealer's flock. A total of 18 commercial layer flocks, two commercial layer pullet flocks, and a commercial meat turkey flock were diagnosed with nonpathogenic AI (H7N2) viral infection with an economic loss estimated at between 3 and 4 million dollars. Clinical histories of flocks infected with the disease included respiratory disease, elevated morbidity and mortality throughout the house, egg production drops, depression, and lethargy. A unique gross lesion in the commercial layers was a severe, transmural oviduct edema with white to gray flocculent purulent material in the lumen. Layer flocks on two separate premises were quarantined but permitted to remain in the facilities until cessation of virus shed was determined through virus isolation. Several months later, clinical AI appeared again in these flocks. It is not known whether the recurrence of disease in these cases is due to persistence of the organism in the birds or the environment. In addition to serologic testing and virologic testing by chicken embryo inoculation, an antigen capture enzyme immunoassay was evaluated as a diagnostic tool for AI. Research projects related to disinfection, burial pits, and geographical system technology were developed because of questions raised concerning transmission, diagnosis, and control of nonpathogenic AI (H7N2).
H7N2 low-pathogenicity (LP) avian influenza (AI) virus was isolated from chickens submitted to the Pennsylvania Animal Diagnostic Laboratory System on December 4 and 5, 2001. The cases were from two broiler breeder flocks in central Pennsylvania that had clinical signs of an acute, rapidly spreading respiratory disease. Seroconversion to AI virus was detected on follow-up sampling. Subsequently, H7N2 LPAI virus was isolated in five different broiler flock cases submitted between December 14, 2001, and January 3, 2002. Clinical signs and lesions in broilers, when present, were compatible with multicausal respiratory disease. With the exception of one broiler flock that was processed, birds from all of the virus positive flocks were euthanatized in-house within 11 days of the original case submission date. Increased surveillance of poultry flocks within 10-mile radius zones centered at the foci of the positive farms continued until March 1, 2002. No additional cases were detected.
Characterization of a novel highly pathogenic avian influenza virus from Chile
- D A Senne
- J C Pedersen
- C Mathieu
Senne, D.A., Pedersen, J.C., Mathieu, C., et al., 2002. Characterization of a novel
highly pathogenic avian influenza virus from Chile. In: Proceedings of the
American Veterinary Medical Association, July 13-17, 2002, Nashville, TN.