A view and an overview on the control of avian influenza outbreaks in poultry: (1-6) Mass-culling of birds (personal experience)

Avian influenza virus (AIV) is RNA virus belongs to the family Orthomyxoviridae. In birds, there are 16 HA and 9 NA subtypes with possible combination of 144 HA-NA subtypes (e.g. H1N1, H5N1, H7N7, H9N2, etc.). According to their pathogenicity in chickens, only some strains of H5 and H7 subtypes are able to produce mass morbidity and mortality and thus are classified as highly pathogenic AIV (HPAIV). Meanwhile, other AIV subtypes including H5 and H7 are low pathogenic (LPAIV) in poultry producing very mild if any clinical illness. The virus infects a wide range of species at different ages, production sectors and countries. Time is the influenza virus’s quest for continuous replication, evolution and adaptation in poultry and mammals. Introduction of an AIV in commercial poultry sectors where a huge number of birds and sometimes mixed species are kept provides optimum condition for the virus replication. In contrast to other viruses in poultry such as infectious laryngotracheitis virus (ILT), Newcastle disease virus (NDV), adenovirus (e.g. egg drop syndrome virus), avian metapneumovirus (TRT), or infectious bursal disease virus (Gumboro disease), the mutation rate of influenza virus is high. The virus requires less than 12 hours for a successful life cycle and release of the progeny viruses from infected cells. Theoretically, with every replication cycle each new virus differs probably from the parent virus by one or more mutation, which may be later fixed or eliminated during the evolution process of the virus. Therefore, influenza virus is considered the master of mutability among other viruses of importance for the poultry veterinary health. Long term endemicity of influenza virus likely leads to efficient replication and adaptation in different hosts, environment and conditions. In addition to the severe losses in poultry industry, the virus has a significant zoonotic importance and poses a potential pandemic risk which should not be underestimated. Therefore, depopulation of infected poultry is an ultimate tool to eradicate the disease rapidly before further spread to other animals and human which is the core principle for depopulation of infected poultry as an intervention strategy. Subsequently, the chances for transformation either to high virulent or transmissible forms in poultry and/or the possibility of human infection and subsequently adaptation will be low. On the contrary to HPAIV infection of poultry with LPAIV strains can sometimes be self-limiting and therefore depopulation of infected birds is not common. Also it is mostly voluntary basis not on a national level. However, some LPAIV can cause very high mortality per se or in case of co-existence of other bacteria, viruses or stress factors (e.g. vaccination, harsh environmental conditions, etc.). Importantly, some LPAIV like H5 and H7 viruses can mutate into high virulent forms, H6, H10 or H9 strains have a zoonotic potential while other AIV subtypes may increase diversity of AIV gene pool in the environment.

There is not a sole accredited measure for successful elimination of avian influenza infection especially the HPAIV H5 and H7 in poultry and each control tool has advantages and disadvantages which must be weighed to decrease the socioeconomic impact of the disease. Therefore in order to control the outbreaks effectively by mass culling of poultry, it must be done as fast as possible, accompanied by restriction of movement and with cost-effective interventions.

In-time diagnosis of influenza infection in the first/index case is critical which is sometimes not successfully done, thus the risk for large-scale spreading of infection in poultry is very high. In some cases, laboratory diagnosis can take several days giving enough time to loose control measures, rise panic, or even smuggling of poultry. At this point, the “bill” of mass culling of poultry becomes more and more expensive. Also, in developing countries the poultry industry grows rapidly and randomly. Culling of poultry in high densities or even in widespread infection in small farms (5000 - 10,000 birds) is not a fast process. In some cases, in an operation with a capacity of 500,000 layer chickens and over 100 part-time workers in a highly poultry and human populated area required more than two months to kill the birds, bury them, dispose the litter and to complete post-culling cleaning and disinfection activities.

One of the important aspects for influenza virus transmission in poultry is the movement of objects (vehicles, animals, people, etc.) from one place to another. In the absence of full restriction of movement, mass-culling of poultry is an ineffective tool for the eradication of influenza outbreaks. Controlling the vehicular movement on the main roads is possible. However, in many instances (e.g. deserts) this is out of the question. More commonly, smuggling of diseased birds or legal transmission of asymptomatically infected birds within a country or even between countries is a real challenge for the eradication of an influenza epidemic. In developed countries tracing of poultry could be achieved and movement of poultry and by-products can be restricted. On the contrary, the infection of poultry in developing countries spread rapidly due to random development of poultry establishments, random movement of people and animals and social-cultural-and-economic circumstance in those countries.

The common test-and-slaughter strategy is to kill infected birds in the infected zone (1 KM radius from the infected farm) followed by a high risk zone (about 2 – 3 KM) where (1) no movement of poultry is allowed (2) surveillance is applied and (3) positive reactors are culled and the third zone is the control zone (up to 10 KM) where sampling occurs. Although sounds ideal this scenario is rarely applicable in developing countries with dense poultry population on limited geographic regions. In the field, many puzzling situations are faced as the availability of updated maps and how to measure the surrounding zones? Should we consider the natural borders (e.g. rivers, mountains, lakes)? What will happen if a breeder farm (over 100,000 birds) is located at the border of the infected zone or close to (≤1 KM) infected backyard birds (less than 10 birds)? What is the “zone” in overlapping infected/high risk zones situation (e.g. if a new outbreak occurred at the border of the first infected zone)? How to control part-time workers and/or their backyard birds? In layer operations, how to convince the culling crow before the owner that the eggs must be also disposed? Most of these decisions must be taken appropriately and rapidly mostly by young veterinarians before others (farm workers, municipalities, policemen, army, etc.) join the cascade. Importantly, protection of participants in the culling-campaign from either legal consequences or risk for exposure to the virus is a great matter of concern.

Additionally, avian and non-avian species in the affected area may play a role in the spread of the infection. For example: infection of feral birds has been repeatedly reported such as sparrows, crews, egrets, herons, and in very few occasions pigeons/doves were found to be infected. Also several animals were found to be susceptible either under natural or experimental infections like dogs, cats, donkeys, cattle, mice, etc. Regardless of their mechanical role, the biological role of these animals in the epidemiology of AIV in poultry has not been fully understood and subsequent control actions are not settled yet (i.e. whether those animals should be also killed or not). In the absence or insufficient biosecurity measures, control of these animals is more difficult.

Costs for rapid and successful depopulation of birds during an outbreak are extremely high. In developed countries these costs may be covered by the industry or the government. However, in developing countries these costs and also post-outbreak cleaning and disinfection is fully or partially paid by the owner which overwhelms the financial status of farmers and prevent or reduce their full and rapid cooperation. In the absence of fair compensation the situation becomes more and more difficult.

Mass depopulation of infected poultry is associated with “mass” criticism from several entities; culling of healthy birds in the infected zone is criticized more and more. Animal welfare organizations consider mass culling of poultry as a violation of animal rights. The media sends mostly negative messages to the population increasing the consumer panic which affects directly the consumption and marketing of poultry. Also, some politicians or executives are against the mass culling of poultry due to political or economic reasons. Members of the industry themselves push the decision makers toward less-expensive approaches. Families in rural areas are completely against killing their birds.

Together, there is a need to include or combine other (alternative or complimentary) approaches to the test-and-slaughter campaign especially in developing countries. This will be overviewed in the next articles.