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Avian influenza (AI) is a disease of viral etiology that ranges from a mild or even asymptomatic infection to an acute, fatal disease of chickens, turkeys, guinea fowls, and other avian species, especially migratory waterfowl


Fowl plague was described in 1878 as a serious disease of chickens in Italy. It was determined in 1955 that fowl plague (FP) virus is actually one of the influenza viruses. The AI viruses, along with the other influenza viruses, make up the virus family Orthomyxoviridae. The virus particle has an envelope with glycoprotein projections with hemagglutinating and neuraminidase activity. These two surface antigens, hemagglutinin (HA) and neuraminidase (NA), are the basis of describing the serologic identity of the influenza viruses using the letters H and N with the appropriate numbers in the virus designation e.g., H7N2. There are now 15 hemagglutinin and 9 neuraminidase antigens described among the Type A influenza viruses. The type designation (A, B, or C) is based upon the antigenic character of the M protein of the virus envelope and the nucleoprotein within the virus particle. All influenza viruses affecting domestic animals (equine, swine, avian) belong to Type A, and Type A influenza virus is the most common type producing serious epidemics in humans. Types B and C do not affect domestic animals. Classical fowl plague viruses have H7 as one of the surface antigens but can have different N antigens. It was once believed that all H7 viruses are highly pathogenic fowl plague viruses and that no other avian influenza viruses could produce a fowl-plague-like disease. When avirulent AI viruses with the H7 antigens were demonstrated in turkeys in 1971 and highly virulent AI viruses with the H5 antigen were first found in chickens in 1959, the necessity for redefining the term fowl plague or using other terminology became apparent. Because there are highly virulent AI viruses that possess H antigen other than the H7 and H7 AI viruses that do not produce clinical fowl plague, an international assembly of avian influenza specialists proposed that the term fowl plague no longer be used. They suggested that any AI virus, regardless of its HA designation, meeting specified virulence requirements in the laboratory be designated highly pathogenic avian influenza (HPAI). The criteria that serve as the basis for classifying an AI virus as HPAI has more recently been modified to include molecular considerations such as the type of amino acids at the cleavage site of its HA. This chapter will be limited to describing the HPAI and not the AI viruses of less virulence and pathogenicity.

Host Range Most avian species appear to be susceptible to at least some of the AI viruses. A particular isolate may produce severe disease in turkeys but not in chickens or any other avian species. Therefore, it would be impossible to generalize on the host range for HPAI, for it will likely vary with the isolate. This assumption is supported by reports of farm outbreaks where only a single avian species of several species present on the farm became infected. Swine appear to be important in the epidemiology of infection of turkeys with swine influenza virus when they are in close proximity. Other mammals do not appear to be involved in the epidemiology of HPAI. The infection of humans with an H5 avian influenza virus in Hong Kong in 1997 has resulted in a reconsideration of the role of the avian species in the epidemiology of human influenza

Geographic Distribution Highly pathogenic avian influenza viruses have periodically occurred in recent years in Australia (H7), England (H7), South Africa (H5), Scotland (H5), Ireland (H5), Mexico (H5), Pakistan (H7), and the United States (H5). Because laboratory facilities are not readily available in some parts of the world to differentiate Newcastle disease and HPAI, the actual incidence of HPAI in the world's poultry flocks is difficult to define. It can occur in any country, regardless of disease control measures, probably because of its prevalence in wild migratory waterfowl, sea birds and shore birds. Avian influenza has produced losses of variable severity, primarily in turkeys in the United States, since the mid-1960's. The disease outbreaks in turkeys in the United States have been caused by AI viruses with many of the HA designations. It was in the fall of 1983 that a highly virulent H5 virus produced severe clinical disease and high mortality in chickens, turkeys, and guinea fowl in Pennsylvania. This severe disease, clinically indistinguishable from classical fowl plague, occurred after a serologically identical but apparently mild virus had been circulating in poultry in the area for 6 months. Outbreaks of less virulent AI have frequently been described in domestic ducks in many areas of the world. The AI viruses are often recovered from apparently healthy migratory waterfowl, shore birds, and sea birds worldwide. The epidemiologic significance of these isolations relative to outbreaks in domestic poultry has led to the generally accepted belief that waterfowl serve as the reservoir of influenza viruses

Transmissions There is a considerable body of circumstantial evidence to support the hypothesis that migratory waterfowl, sea birds, or shore birds are generally responsible for introducing the virus into poultry. Once introduced into a flock, the virus is spread from flock to flock by the usual methods involving the movement of infected birds, contaminated equipment, egg flats, feed trucks, and service crews, to mention a few. Preliminary trapping evidence indicates that garbage flies in the Pennsylvania outbreak were sources of virus on the premises of the diseased flocks. Virus may readily be isolated in large quantities from the feces and respiratory secretions of infected birds. It is logical to assume, therefore, that because virus is present in body secretions, transmission of the disease can take place through shared and contaminated drinking water. Airborne transmission may occur if birds are in close proximity and with appropriate air movement. Birds are readily infected via instillation of virus into the conjunctival sac, nares, or the trachea. Preliminary field and laboratory evidence indicates that virus can be recovered from the yolk and albumen of eggs laid by hens at the height of the disease. The possibility of vertical transmission is unresolved; however, it is unlikely infected embryos could survive and hatch. Attempts to hatch eggs in disease isolation cabinets from a broiler breeder flock at the height of disease failed to result in any AI-infected chickens. This does not mean that broken contaminated eggs could not be the source of virus to infect chicks after they hatch in the same incubator. The hatching of eggs from a diseased flock would likely be associated with considerable risk.

Incubation Period The incubation period is usually 3 to 7 days, depending upon the isolate, the dose of inoculum, the species, and age of the bird.

Clinical Signs Infections of HPAI result in marked depression with ruffled feathers, in-appetence, excessive thirst, cessation of egg production, and watery diarrhea. Mature chickens frequently have swollen combs, wattles (See Pictures at Bottom), and edema surrounding the eyes. The combs are often cyanotic at the tips and may have plasma or blood vesicles on the surface with dark areas of ecchymotic hemorrhage and necrotic foci (See Pictures at Bottom ). The last eggs laid, after the onset of illness, are frequently without shells. The diarrhea begins as watery bright green and progresses to almost totally white. Edema of the head, if present, is often accompanied by edema of the neck. The conjunctivae are congested and swollen with occasional hemorrhage. The legs, between the hocks and feet, may have areas of diffuse hemorrhage (See Pictures at Bottom). Respiratory signs can be a significant feature of the disease, depending on the extent of tracheal involvement. Mucus accumulation can vary. It is not unusual in caged layers for the disease to begin in a localized area of the house and severely affect birds in only a few cages before it spreads to neighboring cages. Death may occur within 24 hours of first signs of disease, frequently within 48 hours, or be delayed for as long as a week. Some severely affected hens may occasionally recover. In broilers, the signs of disease are frequently less obvious with severe depression, inappetence, and a marked increase in mortality being the first abnormalities observed. Edema of the face and neck and neurologic signs such as torticollis and ataxia may also be seen. The disease in turkeys is similar to that seen in layers, but it lasts 2 or 3 days longer and is occasionally accompanied by swollen sinuses. In domestic ducks and geese the signs of depression, inappetence, and diarrhea are similar to those in layers, though frequently with swollen sinuses. Younger birds may exhibit neurologic signs.

Gross Lesions Birds that die with the per acute disease and young birds may not have significant gross lesions other than severe congestion of the musculature and dehydration. In the less acute form, and in mature birds, significant gross lesions are frequently observed. They may consist of subcutaneous edema of the head and neck area, which is evident as the skin is reflected . Fluid may exit the nares and oral cavity as the bird is positioned for postmortem examination. The conjunctivae are severely congested occasionally with petechiation. The trachea may appear relatively normal except that the lumen contains excessive mucous exudate. It may also be severely involved with hemorrhagic tracheitis similar to that seen with infectious laryngo-tracheitis. When the bird is opened, pinpoint petechial hemorrhages are frequently observed on the inside of the keel as it is bent back. Very small petechia may cover the abdominal fat, serosal surfaces, and peritoneum, which appears as if it were finely splattered with red paint. Kidneys are severely congested and may occasionally be grossly plugged with white urate deposits in the tubules. In layers, the ovary may be hemorrhagic or degenerated with darkened areas of necrosis. The peritoneal cavity is frequently filled with yolk from ruptured ova, causing severe airsacculitis and peritonitis in birds that survive for 7 to 10 days. Hemorrhages may be present on the mucosal surface of the proventriculus — particularly at the juncture with the gizzard. The lining of the gizzard peels easily and frequently reveals hemorrhages and erosions underneath. The intestinal mucosa may have hemorrhagic areas especially in the lymphoid foci such as the cecal tonsils. The gross lesions are not distinctly different from those observed with velogenic viscerotropic Newcastle disease (VVND). The lesions in turkeys and domestic ducks are similar to those in chickens but may not be as marked.

Morbidity and Mortality The prognosis for flocks infected with HPAI is poor. Morbidity and mortality rates may be near 100 percent within 2 to 12 days after the first signs of illness. Birds that survive are usually in poor condition and resume laying only after a period of several weeks


Field Diagnosis Highly pathogenic avian influenza is suspected with any flock where sudden deaths follow severe depression, inappetence, and a drastic decline in egg production. The presence of facial edema, swollen and cyanotic combs and wattles, and petechial hemorrhages on internal membrane surfaces increases the likelihood that the disease is HPAI. However, an absolute diagnosis is dependent upon the isolation and identification of the causative virus. Commercially available type A influenza antigen-capture enzyme linked immunosorbent assay kits designed for use in human influenza have recently shown promise as a possible rapid diagnostic test for poultry

Specimens for Laboratory

Specimens sent to the laboratory should be accompanied by a history of clinical and gross lesions, including any information on recent additions to the flock. Diagnosis depends upon the isolation and identification of the virus from tracheal or cloacal swabs, feces, or from internal organs (5). Specimens should be collected from several birds. It is not unusual for many of the submitted specimens to fail to yield virus. Swabs are the most convenient way to transfer AI virus from tissues or secretions of the suspect bird to brain and heart infusion broth or other cell culture maintenance medium containing high levels of antibiotics. Dry swabs should be inserted deeply to ensure obtaining ample epithelial tissue. Trachea, lung, spleen, cloaca, and brain should be sampled. If large numbers of dead or live birds are to be sampled, cloacal swabs from up to five birds can be pooled in the same tube of broth. An alternative technique is to place 0.5 cm3 of each tissue into the broth. Blood for serum should be collected from several birds. If the specimens can be delivered to a laboratory within 24 hours, they should be placed on ice. If delivery will take longer, quick-freeze the specimens and do not allow them to thaw during transit

Laboratory Diagnosis Nine to 11-day-old embryonated chicken eggs are inoculated with swab or tissue specimens. Avian influenza virus will usually kill embryos within 48-72 hours. If the virus isolated is identified as a Type A influenza virus, through the AGP or ELISA tests, it is then tested using a battery of specific antigens to identify its serologic identity (HA and NA type). Sera from infected chickens usually yield positive antibody tests as early as 3 or 4 days after first signs of disease.

Differential Diagnosis Highly pathogenic avian influenza is easily confused with VVND, because the disease signs and postmortem lesions are similar, and may also be confused with infectious laryngotracheitis and acute bacterial diseases such as fowl cholera and Escherichia coli. However, in an area where AI is prevalent, such as during an outbreak, sound presumptive diagnoses can be made by flock history, signs, and gross lesions.

Treatment Amantadine hydrochloride has been licensed for use in humans to treat influenza since 1966. The medication is effective in reducing the severity of influenza Type A in humans. Experimental evidence indicated possible efficaciousness in poultry when the drug was administered in drinking water to reduce disease losses, but drug-resistant viruses quickly emerged, negating the initial beneficial effects. Thus, the drug is not recommended for use in poultry

Vaccination Inactivated oil-emulsion vaccines, although fairly expensive, have been demonstrated to be effective in reducing mortality, preventing disease, or both, in chickens and turkeys (7). These vaccines may not, however, prevent infection in some individual birds, which go on to shed virulent virus. More economical viable vaccines prepared using naturally avirulent or attenuated strains have the disadvantage of the possible creation of reassortant influenza viruses with unpredictable characteristics. These reassortants could result when a single host bird is simultaneously infected with both the vaccine and another AI virus. Owing to the segmented nature of the influenza virus genome, a reassortment of genetic material can readily occur, creating new influenza viruses. The basic drawback to any vaccine approach for the control of HPAI is the large number of HA subtypes that can cause the disease. Because there is no cross-protection among the 15 known HA subtypes, either a multivalent vaccine will be needed or vaccination postponed until the prevalent disease-causing subtype in the area is identified. A recombinant fowl pox virus vaccine containing the gene that codes for the production of the H5 antigen has recently been licensed. The use of a recombinant insect virus containing the gene for either the H5 or H7 antigen has been used to make these vaccine proteins in insect cell cultures

Control and Eradication Wild birds and their excreta should be considered a major source of avian influenza. Preventing direct contact with free-flying birds and protecting domestic poultry from contact with the feces of wild birds is an important way to prevent avian influenza. Live bird markets have been an important source of avian influenza. It is important to avoid live markets, educate employees about the dangers posed by these markets, and prevent the spread of disease from these markets to your flock by preventing any contact. Infected birds shed virus in saliva, nasal secretions and feces in the first two weeks of infection. Four weeks after infection, virus can no longer be detected. Hence, prevention is best accomplished by preventing contact between newly infected and susceptible birds. Biosecurity is a first line of defense. Avian influenza can be spread from infected birds through the transfer of feces especially on contaminated equipment and clothing. Controlling the traffic between infected and uninfected birds is essential.

Cleaning and disinfection Influenza viruses are very sensitive to most detergents and disinfectants. They are readily inactivated by heating and drying. However, flu viruses are well-protected from inactivation by organic material and infectious virus can be recovered from manure for up to 105 days. Complete removal of all organic material is part of any effective disinfection procedure. Contaminated houses are heated for several days to inactivate virus. Organic material is removed followed by complete cleaning and disinfection of all surfaces. Contaminated litter and manure is problematic and should be composted or buried to ensure that it does not spread infectious virus.

Frequently asked questions 1. Are the flu viruses of human and birds the same? In most cases, the influenza viruses that infect birds do not infect humans and vice versa. However, in Hong Kong in 1997, a unique avian influenza virus infected both chickens and humans. This is the only time an avian influenza virus has ever been transmitted directly from birds to humans. This appears to have been a totally unique occurrence. The World Health Organization continuously monitors human influenza viruses isolated from cases all over the world. No avian viruses have been found infecting humans since 1997. 2. What are the risks of getting avian influenza from waterfowl? Avian influenza virus infections are widespread in wild birds, especially ducks. Migrating waterfowl are a significant source of avian influenza viruses especially in the major flyways. Turkeys on open ranges in Minnesota, a state in the major flyway for migrating ducks, frequently experience avian influenza problems. But the prevalence of avian influenza in turkeys has been high in some years and minimal in others. The reason why influenza viruses come and go is not known. The risk to susceptible birds from contact with waterfowl must be considered very high although it may vary from year to year for unknown reasons.3 Why can't I prevent infection by vaccinating my flocks?  Vaccines effectively prevent clinical signs of influenza infections in many species including poultry. However, the vaccines are not cross-protective for the 15 virus subtypes that can infect poultry. Since there is no way to predict which type will infect a flock, vaccines are generally not practical to prevent infections. 4. What should I do if I suspect avian influenza in my birds? You should contact your veterinarian if you observe any of the signs of avian influenza, especially if they are accompanied by a drop in feed consumption and/or a significant drop in egg production. Because the signs of avian influenza are so variable, it is important to get the help of an expert for diagnosis.

Avian Influenza Type A influenza viruses can infect several animal species, including birds, pigs, horses, seals and whales. Influenza viruses that infect birds are called “avian influenza viruses.” Birds are an especially important species because all known subtypes of influenza A viruses circulate among wild birds, which are considered the natural hosts for influenza A viruses. Avian influenza viruses do not usually directly infect humans or circulate among humans. Influenza A viruses can be divided into subtypes on the basis of their surface proteins — hemagglutinin (HA) and neuraminidase (NA). There are 15 known H subtypes. While all subtypes can be found in birds, only 3 subtypes of HA (H1, H2 and H3) and two subtypes of NA (N1 and N2) are known to have circulated widely in humans. Avian influenza usually does not make wild birds sick, but can make domesticated birds very sick and kill them. Avian influenza A viruses do not usually infect humans; however, several instances of human infections and outbreaks have been reported since 1997. When such infections occur, public health authorities monitor the situation closely because of concerns about the potential for more widespread infection in the human population.

Avian Influenza Infections in Humans: Confirmed instances of avian influenza viruses infecting humans since 1997 include:

1997: In Hong Kong, avian influenza A (H5N1) infected both chickens and humans. This was the first time an avian influenza virus had ever been found to transmit directly from birds to humans. During this outbreak, 18 people were hospitalized and 6 of them died. To control the outbreak, authorities killed about 1.5 million chickens to remove the source of the virus. Scientists determined that the virus spread primarily from birds to humans, though rare person-to-person infection was noted. 1999: In Hong Kong, cases of avian influenza A H9N2 were confirmed in 2 children. Both patients recovered, and no additional cases were confirmed. The evidence suggested that poultry was the source of infection and the main mode of transmission was from bird to human. However, the possibility of person-to-person transmission remained open. Several additional human H9N2 infections were reported from mainland China in 1998-99. 

2003: Two cases of avian influenza A (H5N1) infection occurred among members of a Hong Kong family that had traveled to China. One person recovered, the other died. How or where these 2 family members were infected was not determined. Another family member died of a respiratory illness in China, but no testing was done. No additional cases were reported.

2003: Avian influenza A (H7N7) infections among poultry workers and their families were confirmed in the Netherlands during an outbreak of avian flu among poultry. More than 80 cases of H7N7 illness were reported (the symptoms were mostly confined to eye infections, with some respiratory symptoms), and 1 patient died (in a veterinarian who had visited an affected farm). There was evidence of some human-to-human transmission.

2003: H9N2 infection was confirmed in a child in Hong Kong. The child was hospitalized but recovered

Characteristics of Avian Influenza in Birds: Certain water birds act as hosts of influenza viruses by carrying the virus in their intestines and shedding it. Infected birds shed virus in saliva, nasal secretions and feces. Avian influenza viruses spread among susceptible birds when they have contact with contaminated nasal, respiratory and fecal material from infected birds; however, fecal-to-oral transmission is the most common mode of spread. Most influenza viruses cause no symptoms, or only mild ones in wild birds; however, the range of symptoms in birds varies greatly depending on the strain of virus and the type of bird. Infection with certain avian influenza A viruses (for example, some H5 and H7 strains) can cause widespread disease and death among some species of wild and especially domesticated birds such as chickens and turkeys. Symptoms of Avian Influenza in Humans The reported symptoms of avian influenza in humans have ranged from typical influenza-like symptoms (e.g., fever, cough, sore throat and muscle aches) to eye infections, pneumonia, acute respiratory distress, viral pneumonia, and other severe and life-threatening complications. Antiviral Agents for Influenza Studies to date suggest that the prescription medications approved for human influenza strains would be effective in preventing avian influenza infection in humans, however, sometimes flu strains can become resistant to these drugs and so they may not always be effective.

Potential for an Influenza Pandemic: All influenza viruses can change. It is possible that an avian influenza virus could change so that it could infect humans and could spread easily from person to person. Because these viruses do not commonly infect humans, there is little or no immune protection against them in the human population. If an avian virus were able to infect people and gain the ability to spread easily from person to person, an “influenza pandemic” could begin.

Background on Pandemics An influenza pandemic is a global outbreak of influenza and occurs when a new influenza virus emerges, spreads, and causes disease worldwide. Past influenza pandemics have led to high levels of illness, death, social disruption and economic loss. There were 3 major pandemics in the 20th century. All of them spread worldwide within 1 year of being detected. They are:

1918-19, "Spanish flu," [A (H1N1)], caused the highest number of known flu deaths: more than 500,000 people died in the United States, and 20 million to 50 million people may have died worldwide. Many people died within the first few days after infection and others died of complications soon after. Nearly half of those who died were young, healthy adults.

1957-58, "Asian flu," [A (H2N2)], caused about 70,000 deaths in the United States. First identified in China in late February 1957, the Asian flu spread to the United States by June 1957.

1968-69, "Hong Kong flu," [A (H3N2)], caused approximately 34,000 deaths in the United States. This virus was first detected in Hong Kong in early 1968 and spread to the United States later that year. Type A (H3N2) viruses still circulate today. Once a new pandemic influenza virus emerges and spreads, it typically becomes established among people and circulates for many years. The U.S. Centers for Disease Control and Prevention and the World Health Organization conduct extensive surveillance programs to monitor the occurrence of influenza activity worldwide, including the emergence of potential pandemic strains of influenza virus. For this reason, public health concerns about the present H5N1 situation must be given the highest priority when weighing the immediate and measurable economic losses in animals against possible yet unpredictable consequences for humans. Several other diseases in animals can be transmitted to humans. Experience with such diseases, known as “zoonoses”, has shown that strict measures on animal health, imposed by the need to protect human health, helped rebuild consumer confidence. Recent experience has also shown that measures for the control of zoonotic diseases, aimed at halting further spread in animals and minimizing economic losses, need to be closely coordinated with measures that minimize the longer-term risks to human health. In the present situation, measures aimed at eliminating the disease in poultry will also reduce the presence of the virus in the environment and thus reduce opportunities for human exposures and infections. These measures must be carried out urgently, giving highest priority to the protection of human health. Previous outbreaks of highly pathogenic avian influenza associated with human infections occurred in areas, such as Hong Kong and the Netherlands, with industrial poultry production and well developed health and agricultural infrastructures. Even so, elimination of infection in poultry was a complex, difficult, and costly undertaking. Both outbreaks were eventually controlled through immediate culling of infected flocks, quarantine and disinfection of farms, strict biosecurity, restrictions on the movement of animals, and compensation for farmers. The present situation is different. Control of outbreaks of highly pathogenic avian influenza is known to be especially difficult in areas where poultry range freely. In several affected countries, up to 80% of the total poultry population is raised in small backyard farms. Most rural families keep a small free-range flock. Given these features of the present situation there is potential that the H5N1 virus could become established in bird populations in this geographical region and possibly spread to other parts of the world. This was one of several conclusions reached during a joint FAO/OIE/WHO technical consultation on the control of avian influenza, held in Rome from 3–4 February. No single blueprint for control in animals, and thus reduction of risks for humans, is available. Over the past four decades, only 18 outbreaks of highly pathogenic avian influenza, most caused by strains other than H5N1, have occurred throughout the world. Existing evidence will not suffice to provide universally applicable recommendations for a rapid and effective response in affected countries. Control measures must be tailored to each country’s unique epidemiological situation and unique capacity, with health and agricultural sectors working hand-in-hand. Agricultural authorities face the immediate challenge of rapidly eliminating the H5N1 reservoir in poultry. Authorities in all affected countries need to work together in a coordinated way Transparency in reporting of human and animal disease is absolutely essential. Despite the uncertainties, experts fully agree that immediate culling of infected and exposed birds is the first line of defense for both the protection of human health and the reduction of further losses in the agricultural sector. Other measures, such as the vaccination of healthy flocks, may play a supportive role in some cases when undertaken in conjunction with measures for preventing further spread of infection. WHO has repeatedly stressed the need to ensure that culling  is carried out in a way that does not fuel more human cases. and that vaccination of poultry should not lead to the dropping of vigilance or compromise other necessary control measures. In responding to the situation, WHO emphasises three strategic goals: to avert an influenza pandemic, to control the present human outbreaks and prevent further spread, and to conduct the research needed for better preparedness and response, including the immediate development of a new vaccine for humans against H5N1. WHO has issued a series of technical guidelines aimed at minimizing the risk of further human cases and facilitating a coordinated international response. Highly pathogenic avian influenza is categorized by OIE as a “list A” disease. List A includes transmissible diseases “which have the potential for very serious and rapid spread, irrespective of national borders, which are of serious socio–economic or public health consequence and which are of major importance in the international trade of animals and animal products.” One example is the spread of bovine spongiform encephalopathy, or “mad cow disease”, in cattle, which led to the emergence of a rare yet invariably fatal new disease in humans.









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