Content uploaded by Muhammad Mobashar
Author content
All content in this area was uploaded by Muhammad Mobashar on Jan 09, 2025
Content may be subject to copyright.
ZOONOSIS
42
Dissemination of Highly Pathogenic Avian Influenza through Wild
Migratory Birds
Muhammad Zubair Arshad1*, Muhammad Mobashar2, Bushra Zaidi3, Talha Shabbir4, Abdullah
Shahab6 and Amna Kanwal1, Atif Rehman1* and Muhammad Subbayyal Akram6
ABSTRACT
Avian influenza viruses (AIVs) pose a significant threat to both poultry and human populations due to
their ability to cross species barriers. This review explores the genetic diversity and factors influencing
the pathogenicity of Influenza A viruses, focusing on the H5N2 subtypes currently circulating in China.
The viral subtypes are determined by Neuraminidase (NA) and Hemagglutinin (HA) genes, with H5N2
variants dominating recent outbreaks. The presence of polybasic cleavage sites in the HA molecule is a
key indicator of high pathogenicity. Notably, the NP, PB1, and PB2 proteins contribute to increased
pathogenicity. Outbreaks are classified based on cytotoxicity and the presence of polybasic cleavage
sites in the HA. The dissemination of AIVs is closely linked to wild birds, especially migratory species.
HPAI spread through migratory flyways, raising concerns about cross-continental transmission. The
study addresses the role of migratory birds, exploring questions regarding their ability to carry
infections while migrating and the involvement of illegal exotic bird trade in viral spread. Surveillance
measures are crucial for early detection and preparation, necessitating updated kits and knowledge
about wild bird behavior. The global impact of AIVs on the poultry industry is profound, affecting both
small and large-scale farmers. Economic losses, culling practices, and societal impacts are discussed,
emphasizing the vulnerability of small-scale farmers in developing countries. Prevention strategies
involve understanding migratory patterns, implementing effective surveillance, and preparing
management protocols. Coordination among organizations and heightened situational awareness are
vital components of proactive measures against AIV outbreaks.
Key words: Avian influenza, Genetic diversity, Migratory birds, Viral reassortment, Surveillance
CITATION
Arshad MZ, Mobashar M, Zaidi B, Shabbir T, Shahab A, Kanwal A and Akram MS, 2023. Dissemination of
highly pathogenic avian influenza through wild migratory birds. In: Aguilar-Marcelino L, Zafar MA, Abbas
RZ and Khan A (eds), Zoonosis, Unique Scientific Publishers, Faisalabad, Pakistan, Vol 3: 42-51.
https://doi.org/10.47278/book.zoon/2023.84
CHAPTER HISTORY
Received:
26-Feb-2023
Revised:
25-May-2023
Accepted:
14-Nov-2023
1Department of Pathology, University of Agriculture Faisalabad, Pakistan.
2Department of Animal Nutrition, The Universuty of Agriculture Peshawar- Pakistan
3Department of Clinical Medicine and Surgery University of Agriculture Faisalabad, Pakistan.
4Department of Microbiology, University of Agriculture Faisalabad, Pakistan.
5Faculty of Veterinary Science, University of Agriculture Faisalabad, Pakistan.
6Department of Parasitology, University of Agriculture Faisalabad, Pakistan
7Department of Poultry Science, MNS University of Agriculture, Multan
*Corresponding author: zubairarshad202@gmail.com; atif.rehman@mnsuam.edu.pk
04
ZOONOSIS
43
1. INTRODUCTION
The Influenza A virus (IAV) has the broadest range of hosts and carries extraordinary gene diversity
compared to the other two influenza virus types (Zhang et al. 2013). The subtypes of influenza viruses
are determined by their Neuraminidase (NA) and Heam-agglutinin (HA) genes, of which there are 18
and 11 forms, respectively. These viruses have a history of infecting avian hosts, as evidenced by
analysis of their viral genomes using phylogenetic link. Although the presence of a site for polybasic
cleavage on the HA of H5 viruses is an indicator of their high pathogenicity, experiments in chickens
have shown that the introduction of polybasic genes into the LPAIV HA does not necessarily produce
a fatal phenotype (Bogs et al. 2010). NP, PB1, and PB2 Influenza proteins may make it more pathogenic
to an influenza virus.
Classification of Low pathogenic AIV or High Pathogenic AIV outbreaks in poultry often relates to the
cytotoxicity of the infectious agent during illness and if the virus possesses a site for polybasic cleavage
in its HA molecule (as mentioned above). However, other proteins, including NA, can increase the virus's
pathogenicity. Currently, the H5N6, H5N8, and H5N2 viruses of type H5Nx are the newly circulating AIV
strains in China. As a result of these viral re-assortments (Lee et al. 2017). A dominant NA molecule may
emerge, increasing the pathogenicity and viral particle release. Viral modifications in the Hemag-glutinin
proteolytic cleavage site, such as the mutation of numerous non-basic amino acids to basic amino acids,
replication of essential amino acids, or mutation with insertion of viral or cellular amino acids, have led
to the emergence of high-pathogenic avian influenza (HPAI) viruses from low-pathogenic avian influenza
(LPAI) viruses (Swayne et al. 2016). The first cases of the highly pathogenic avian influenza virus in
poultry birds were discovered in northern Italy in 1878 (Swayne et al. 2016). Six people died in Hong
Kong in 1997 after being infected with the H5N1 strain of the highly pathogenic avian virus (HPAIV),
which was first discovered in 1996 in China. The H5 clade 2.3.4.4 (HPAI) subtype H5N8 virus was first
identified in chickens in South Korea in 2014. In Europe, North America, and Asia, by the middle of 2015,
it has spread to domestic and wild birds (Hall et al. 2015).
2. SUBTYPES
At present, AI viruses can contain surface proteins from any of the nine different neuraminidase
subtypes (N1-9) and the 16 different Hemag-glutinin subtypes (H1-16) (Swayne et al. 2016).
2.1. AVIAN INFLUENZA A(H5) VIRUSES
There are nine different subtypes of the A (H5) virus including (H5N1), (H5N2), (H5N3), (H5N4), (H5N5),
(H5N6), (H5N7), (H5N8) and (H5N9) (Swayne et al. 2016).
2.2. AVIAN INFLUENZA A (H6) VIRUSES
A (H6) viruses have several subtypes, including LPAI A (H6N1) and A (H6N2). The first known human LPAI
A (H6N1) virus infection was reported in Taiwan in 2013 (Swayne et al. 2016).
2.3. AVIAN INFLUENZA A (H7) VIRUSES
The nine subtypes of AIV
A (H7N1), A (H7N2), A (H7N3), A (H7N4), A (H7N5), A (H7N6), A (H7N7), A (H7N8) and A (H7N9) are all
currently recognized (Swayne et al. 2016).
ZOONOSIS
44
2.4. AVIAN INFLUENZA A (H9) VIRUSES:
There are nine recognized subtypes of AIV: A (H9N1), A (H9N2), A (H9N3), A (H9N4), A (H9N5), A
(H9N6), A (H9N7), A (H9N8) and A (H9N9). All A (H9) viruses seen in wild birds and poultry across the
world are LPAI viruses (Swayne et al. 2016).
2.4.1. AVIAN INFLUENZA A (H10) VIRUSES
A (H10) viruses come in a variety of subtypes, including:
A (H10N3), A (H10N4), A (H10N5), A (H10N6), A (H10N7) and A (H10N8). In 1984, a mink was reported to
have A (H10N4), and in 2008, swine (pigs) were found to have A (H10N5). A (H10N3), A (H10N7) and A
(H10N8) are the A (H10) virus subtypes reported to have infected humans (Swayne et al. 2016).
3. RECENT OUTBREAKS
When it affects the poultry population, the avian influenza virus (AIV) can lead to severe epidemics
(James 2000). However, it occasionally infects people who come into contact with infected birds. A
particular illness that has spread beyond its expected endemicity is said to be an epidemic when there
are more instances than typical (King et al. 2021). A specific number of cases, meanwhile, is not
necessarily required for there to be an epidemic (Bellouet al. 2013). Aside from that, identifying an
epidemic also heavily depends on the moment and location of occurrence. So, an epidemic belongs to a
particular group of people (community), in a specific place (geographical area) and at a special moment
in time (season) (Marchenkoet al. 2011). Since the Gs/GD HPAI viruses first emerged (in 2002), in the
outbreaks of HPAI, East Asia has played a significant geographic role that frequently affects aquatic birds
in the wild and in captivity (Marchenkoet al. 2015).
Russia, Japan and South Korea are among the nations in East Asia that have frequently been impacted
by previous HPAI epidemics in wild birds (Sakodaet al. 2012). In the 20th century, in 1918, 1957, and
1968, three influenza pandemics occurred, resulting in about 0.5 million, 1 million and 05 million
fatalities. AIV subtype H5N1 is still the most prevalent subtype. Additionally, the most common region
for the geographic scope of epidemics is Asia. A number of the most significant pandemics between
2010 and 2016 were counted in Taiwan, South Korea, China, Japan, India, Israel, and Vietnam. It’s due to
enhanced clinical and laboratory programs conducted in all of these nations over the past few years, or
it may be because these nations have a distinctive environment with plenty of lakes, rivers, creeks,
ponds, and creeks that serve as wintering grounds for migratory birds (Jeonget al. 2014).
Cases with a more significant percentage were recorded in Egypt (including Cameroon, Nigeria, Africa,
Togo, Libya, Tunisia, Ghana, Burkina Faso, and Cote d'Ivoire). The Spread of the virus in Europe,
particularly HPAI H5N8 emergence in Germany, has reinforced the intimate connection between the
habitats of wild birds and the pathogen dissemination through their migration (King et al. 2021). The
greatest H5N2 epidemic ever documented in the United States occurred between 2014 and 2015, and to
stop the expansion of the disease, almost 51 million birds were depopulated. Twenty-five million birds,
or 409,836 every day or 284 per minute, were killed between May and June 2015 in the United States
(Chatziprodromidouet al. 2018).
The government spent a total of US$879 million during the 2014–2015 H5N2/H5N8 epidemic, while
more than US$3 billion was paid by the United States egg and poultry industries to stop the disease
from infecting poultry. In the USA, this HPAI outbreak was the most expensive. Due to the new wave of
HPAI H5N8 viruses in numerous European nations saw severe outbreaks of wild and poultry birds in the
first half of 2020 (Jacobs 2022).
ZOONOSIS
45
There were many bird flu outbreaks reported in Europe before the end of 2020. (HPAI) High-pathogenic
avian influenza virus outbreak has been detected in numerous European nations since mid-October,
primarily in wild birds, including Germany, France, Belgium, Sweden, Denmark, Ireland, the United
Kingdom and Netherlands (Hall et al. 2015). Other poultry and captivity birds tested positive as well.
Three different types of Highly pathogenic avian influenza viruses, A(H5N1), A(H5N5), and A(H5N8),
were discovered, with H5N8 being the most often found, declared by the European Center for Disease
Prevention and Control (ECDC). To stop the H5N8 virus from spreading, 29,000 hens were slaughtered in
Germany (Lee et al. 2020).
4. UNITED STATES 2022–23 OUTBREAK
All Health Monitoring Agencies working for the betterment of public health in the United States
collaborated and worked on the pandemic wave. Data came on board revealing that a single wave of the
viral activity resulting in deaths of many birds following the second wave which came around the end of
2022 which impacted the major Nine areas of the America (Merced-Morales et al. 2021). Despite strict
prevention strategies put in place by the sector following the 2015 outbreak, the most recent outbreak
has cost about $661 million to the government, and there is no control to the outbreak in sight (Cox et
al. 2000).
4.1. AFRICA 2023 OUTBREAK
In Early December 2020, in the poultry shed rearing, the total number of birds was almost more than 0.1
million. In a small village area of Africa, suddenly, this poultry farm showed numerous mortalities, which
created an alarming situation in the Area. The clinical signs and symptoms reported in the birds affected
by that infection were swelling of the neck, the pale coloration of the body parts, and congestion in the
respiratory (Lo et al. 2022). Given that wild birds in North America that are a carrier of Gs/GD HPAI
viruses gives some amount of health danger to people who interact with domestic and wild animals, it is
essential for efficient coordination to occur across management organizations and agencies for wildlife,
agriculture, and public health (Sleemanet al. 2017).
5. DISSEMINATION THROUGH MIGRATORY BIRDS
In the research and studies conducted on the widespread of highly pathogenic AIV, there is a critical talk
about its dissemination through the migratory routes of the wild birds. The burning issue is H5N1 spread
to the European countries and is thought to be due to the fly routes of the birds (Kilpatrick et al. 2006).
Whenever there is a talk about the pandemic of HPAI strain H5N1 from Asia to the countries of Europe,
the only culprit is not the wild birds. We also need to shed a light on the illegal movement of exotic and
wild birds and the movement of poultry products through international trade routes (Salzberget al.
2007). Wild birds, which have the nature of migration in their life from Europe to Asia and other
countries like Russia and North America, are the central spreading element of the H5N1 virus in
pandemics (Feare2007; Gauthier-Clercet al. 2007).
Two significant concerns arise here, which are required to be addressed first, as wild birds are the most
discussed element of dissemination for HPAI, but if they get infected with the virus, are they still able to
migrate to carry infection? Till now, the answer to this question is not available, as supporting research
is silent (Flint 2007). In some studies, it was seen that HPAI infection, especially the Asian strain, does
not cause mortality in some wild bird species, like water-fowls (Brown et al. 2006; Keawcharoenet al.
ZOONOSIS
46
2008). The second question that needs to be answered is that the fly routes of the wild migratory birds
are really involved in the dissemination of highly pathogenic types of AIV between the continents and
causes pandemics in Europe and North America. There is another point to be noted that many
outbreaks of the HPAI virus in wild birds were not the dissemination root cause, which revealed that the
new areas where the HPAI pandemic occurs is not linked with the migration behavior of the wild birds
which carry H5N1 Infection (Kalthoffet al. 2008).
Various zoonotic infections are disseminated over long distances and change their shape to pandemics
through the wild migratory birds when they carry them during their migration from one place to another
(Reed et al. 2003). During the regular fly pattern between continents, the most spreading agent is AIV,
which is transmitted to long distances via these wild birds (Olsen et al. 2006; Lam et al. 2012).
Low pathogenic type of AIV is usually transferred to long distances during the migration of wild water-
fowls (Webster et al. 1992), and these birds carry this low pathogenic strain to other continents like
Africa and America (Cappelleet al. 2012). One question still requiring attention: as is there any regional
spread of the AIV virus through these wild types of flying birds in the regions? (Normile2005; Hill et al.
2012). The first case of HPAI was reported in Asia in the last of 1995 (Li et al. 2004), which was then seen
to spread through the migration of wild birds in other continents, causing many economic losses and
taking human lives as well. It was seen that the rate of transmission of HPAI type of H5N1 from birds to
Humans and then its transmission from humans to humans itself was not that significant.
The mortality rate was higher, which is why it was widespread among the wild birds and was a serious
issue for the human health committees (Webster et al. 2006). Qinghai Lake was the breeding ground for
many wild birds that migrate towards other continents, and that’s why the particular strain of HPAI
H5N1 transmitted to other areas through the wild birds from the lake area (Brown et al. 2008). It was
also noted that many birds, after carrying the infection, sometimes don’t show any infection as they
migrate and shed the virus without showing any signs and symptoms of H5N1 (Keawcharoenet al. 2008).
The take-home message was that large-scale transmission of HPAI infection through migratory birds
isn’t that easy to detect (Gaidetet al. 2008).
6. INFLUENZA THROUGH WATERBIRDS
Many water birds carry infectious viruses, which may be zoonotic, as dabbling ducks and mallards carry
avian influenza virus (Olsen et al. 2006). Almost all the antigenic different types, including Hemag-
glutinin and neuraminidase, are seen in the dabbling ducks (Fouchier et al. 2005; Olsen et al. 2006;
Krauss et al. 2004; Latorre-Margalefet al. 2009). The incidence of occurrence of infection of avian
influenza virus in the mallards ranges from 10% in the hot season while it can vary to 60% in the fall
season, and this is seen in both nearby continents like Asia and Europe and the northern side of America
(Olsen et al. 2006; Krauss et al. 2004; Latorre-Margalefet al. 2009; Wallenstenet al. 2007). This kind of
variation may be due to many factors which influence the viral spread and its survival. Factors including
the breeding season and the other environmental elements which harbour the viral replication and its
widespread are made possible (Stallknechtet al. 1990).
6.1. INFLUENZA THROUGH SHOREBIRDS
Charadriiformes is the class of birds which is found to be a habitat on many continents. Which may be
many types of birds named as gulls and terns. It is also seen that the frequency and prevalence of the
HPAI type of influenza is little different in Charadriiformes than in the Anseriformes (Kawaokaet al.
1998).
ZOONOSIS
47
The unique point about the Charadriiformes is that two subtypes are only seen in those birds, which are
H13 and H16 (Krauss et al. 2004). Another unique point is the shore birds show HPAI infection most of
the hot summers (Kawaokaet al. 1998). Ducks have a different pattern of moving to their breeding
grounds compared to other shore birds. While most shore birds migrate during the summer, ducks
migrate during the fall season. This leads to a higher transmission of infections during this time for ducks
(Stallknechtet al., 1988). Hence, the purpose of this talk is the type of birds living in shore areas of the
world are seen to be more important in breeding grounds and for longer periods the presence of
infection in the wild type of birds may be important as the transmit the infection during their migration
to the northern areas of the world in spring (Lee, et al., 2015).
Many studies conducted on the prevalence and frequency of infection in the Charadriiformes and
Anseriformes showed different patterns of infection in both (Tian et al. 2015). In a study conducted, a
total of 63 subtypes with the HA and NA genes were detected in more than 13 thousand samples of
shore birds in almost 15-16 years (Tian et al. 2015). Two different orders of birds including Anseriformes
(geese, swans and ducks) and Charadriiformes (gulls and shorebirds), are the names of wild birds. For
the low pathogenic type of HPAI virus type A, wild birds are major dissemination elements (Leeet al.
2017). Ruddy shelducks, great black-headed gulls, great cormorants, bar-headed geese, brown-headed
gulls, and common coots in Qinghai Lake are common wild birds (Tian et al. 2015).
When the wild birds migrate on their usual fly routes, it is seen that there are some stopover places for
their preparation for next migration (Kim et al. 2009), and they seem to get infected in those places by
the domestic poultry in nearby places (Tian et al. 2015). Sanmenxia Clade type 2.3.2.1c-like HPAI virus
seemed to spread through this way of migration of wild birds (Li et al. 2014). Countries in Europe and
Asia, including Japan, China, Korea and Eastern Europe (Eurasia), are best breeding grounds for wild
birds like whooper swans (Uchida et al. 2008). numerous whooper swans which have their breeding
ground in China and complete their wintering on that ground (Almost 20,000 birds). More than 10000
birds from the total during their migration breed on the grounds of Sanmenxia, where ducks of East
Asian sides also stay and breed. Their migration isn’t complete on those grounds, but after arriving in
October on Sanmenxia lake, they fly back to their native grounds in Mongolia and Siberia for next spring
breeding (Aoet al. 2020).
In Russia and other neighboring countries like Kazakhstan, Genetic re-assortment of highly pathogenic
avian influenza virus created new research grounds that linked the pandemics of the H5N8 virus in
Europe (in late and early 2020) with these re-assortment strains (Liang et al. 2021).In Asia the studies
show that the spread as the pandemic of HPAI, specially the strain, is due to the wild migratory birds
that disseminate the H5N1 strain (Tian et al. 2015), .and then these migratory birds take the route to
Europe (Xu et al. 2016). Research focusing on the transmission of AIV revealed that the gene flow
usually occurs between the routes of the same region, and usual gene flow occurs through them (Lam et
al. 2012). In another study, it was seen that migratory flyways of individuals or the partial type may be
associated with the gene flow or transmission of AIV through the migration networks (Zhang et al.
2023).
In Early 2015 near the Sanmenxia Lake which is the breeding ground for many migratory wild birds,
including whooper swans and other birds, for example ducks from china and nearby countries like
Siberia and Mongolia. These birds take their migratory route from Qinghai Lake to Sanmenxia reservoir
area. Deaths of more than 100 birds in this area created alarming conditions as it seemed another HPAI
virus outbreak, and this outbreak was connected with the fly routes of the following discussed wild
birds(Swayne et al. 2020).
In the wake of pandemics, dissemination of the virus through wild birds usually occurs, and it is required
to take strict measures about their movement to make surveillance on the virus (Bi et al. 2015). This
ZOONOSIS
48
kind of early surveillance is helpful in early preparation for such widely spreading viruses. For testing
purpose, an updated surveillance kit containing required reagents is needed. Also, new updated
knowledge about the wild bird’s movement and their virus-shedding behavior can answer the questions
about the HPAI ecology, epidemiology, spatial and temporal spread (Fouchier et al. 2005). In a study
conducted in 1997, a total of more than 27 thousand samples were collected in the form of cloacal
swabs and fresh samples of bird droppings. These samples were tested for the presence of the RNA of
HPAI virus type A (Fouchier et al. 2000; Munster et al. 2005). There were two different types of
distribution of samples on the basis of the collection as the majority of the samples were taken from the
different geographical areas of Sweden and the Netherlands. At the same time, other type of collection
was done from the 40 different locations of the world for a pilot study. Wide samples were from the
Seagulls, Water geese, Ducks and from shorebirds but these were not the only species as the samples
were collected from the 250 different species of birds for HPAI surveillance. Samples from the Greylag
Goose, Eurasian Wigeon, Northern Shoveler, Northern Pintail, Common Teal, Black-headed Gull,
Mallard, Common Guillemot and Greater White Goose were seen positive. Overall positive surveillance
ratio for the HPAI virus was 2.1% in wild birds, but it is noted that it may rise to 60% in the specific
geographical areas or the stay points of the wild birds in specific months (Fouchier et al. 2005).
In a study conducted on Northern Pintails (usually takes a fly route between Asia and Northern-areas of
America, and it is evident it has shown higher Asian HPAI lineages frequency in areas of Alaska) very
little evidence of Asian lineage parts was seen even the study was performed on their areas of breeding
(Keawcharoenet al. 2008). It is seen that the genetic base studies done on the Low Pathogenic type of
Avian Influenza can be useful for the decision-making in the area wise study or specie-related spread of
the Highly Pathogenic type of Avian Influenza. It can be understood that if a route of migration of wild
birds or species isn’t found to be the culprit for the spread of Avian Influenza of low pathogenic type, it
will be very unlikely otherwise for the High Pathogenic type. The same if a species or the migration route
seems to support the spread of LPAI, there will be higher Chances of HPAI spread from the same route
or the same bird species. Very high chances of genetic re-assortment of two important genes (HA and
NA) make it very hard to study the normal pattern. Therefore, the recommended way is complete
genetic sequencing, which will open up the surveillance ways for the spread of HPAI pandemics as it will
tell us the normal patterns of genetic re-assortment of the LPAI genes (Koehler et al. 2008).
7. GLOBAL IMPACT
The poultry industry as a major part, capturing the 20% share of total protein source in developing
countries (Alders et al. 2014). In the recent past, due to the Highly Pathogenic type of Avian Influenza
spread across the borders, the killing of millions of birds was practiced to limit the pandemic. Several
control measures in Vietnam resulted in the culling and disposal of over 50 million poultry birds in the
wake of the HPAI pandemic (McLeod et al. 2005). Economic downfall in the year 2005 estimated by the
Food and Agriculture Agency were over billions of Dollars in the East side of the South Asia continent
(McLeod et al. 2005). It is seen that these pandemics have great negative impact on both small and
large-scale farmers, but small-scale farmers raising poultry in the domestic form in villages are affected
greatly than the industrial scale. Industrial-scale farmers face temporary downfall in the form of asset
losses or Market worth. The compensation scenario is different in developing and developed countries
as many get more than their Market. On the contrary, countries like Cambodia provide no support for
affected Farmers (Alders et al. 2014).
In recent past due to the influenza pandemics domestic poultry faced many crises, and the most
affected element of the industry was lower-scale poor farmers (Porter 2012). In developing countries
ZOONOSIS
49
like Vietnam, total losses to the poultry industry, especially to small-scale farmers, were over a hundred
Dollars. Production was also hampered for an average of 2-3 months due to the HPAI pandemic in those
areas where per-day earning is less than the USA $2 (McLeod et al. 2005). Stunted growth is a major
setback in children seen in those areas of Egypt affected by HPAI pandemics. In many countries, small-
scale flocks of poultry are reared by women, and they are impacted by these losses (Bagnol2012). In
Turkey, it was noted that due to widespread cases of HPAI, culling practices in small-scale village areas
rearing domestic poultry resulted in a lower number of school enrolment for girls (Alders et al. 2014).
8. PREVENTION
Highly Pathogenic avian influenza is reported to spread across borders of Europe to Asia. Due to this
widespread circulation, it is necessary to understand the mechanism of its propagation in the form of a
pandemic across Eurasia. During their flight from Europe to Asia, many birds gather at different stay
points, making these geographic regions hot points (Lee, et al., 2015).
Different management strategies by the agencies dealing in hot areas of migratory birds are necessary
to obtain the development and application of action protocols to limit the widespread HPAI outbreak.
Managers of these agencies should be well aware of the migratory patterns and the stay behavior of
wild birds. They should keep a close eye on the type and number of mortality or morbidity during the
migration in order to get prepared for any alarming situation. They should maintain proper surveillance
of the health of these birds on a territorial or provincial level (Leeet al. 2017).
A second possible step towards determining whether and how to develop and apply management
actions to mitigate damages incurred through the dissemination of HPAI via wild birds is to be prepared.
Preparations include numerous elements such as coordination and communication within a
management organization and with external agricultural and public health agency partners,
consideration of the appropriate use of personal protective equipment (PPE) during outbreak events,
determining whether and how to document the geographic extent of HPAI outbreaks in wild birds,
evaluation of management options to mitigate the dissemination or effects of HPAI viruses, and
elevating situational awareness as determined to be appropriate (Lee et al. 2017).
REFERENCES
Alders R et al., 2014. Impact of avian influenza on village poultry production globally. EcoHealth 11(1): 63–72.
AoP et al., 2020. Migration routes and conservation status of the Whooper Swan Cygnus cygnus in East Asia.
Wildfowl Special 6: 43-72.
BagnolB, 2012. Advocate gender issues: A sustainable way to control Newcastle Disease in village chickens. INFPD
Good Practices of Family Poultry Production Note No 03.
BellouM et al., 2013. Shellfish-borne viral outbreaks: a systematic review. Food and Environmental Virology 5: 13–
23.
Bi Y et al., 2015. Highly Pathogenic Avian Influenza A(H5N1) Virus Struck Migratory Birds in China in 2015. Scientific
Reports 5: 1–12.
Bogs J et al., 2010. Highly pathogenic H5N1 influenza viruses carry virulence determinants beyond the polybasic
Hemag-glutinin cleavage site. PLoS One 5: 11826.
Brown JD et al., 2006.Susceptibility of North American ducks and gulls to H5N1 highly pathogenic avian influenza
viruses. Emerging Infectious Diseases 12: 1663–1670.
Brown JD et al., 2008. Experimental infection of swans and geese with highly pathogenic avian influenza virus
(H5N1) of Asian lineage. Emerging Infectious Diseases 14(1): 136–142.
CappelleJ et al., 2012. Circulation of avian influenza viruses in wild birds in Inner Niger Delta, Mali. Influenza and
Other Respiratory Viruses 6(4): 240–244.
ZOONOSIS
50
Chatziprodromidou IP et al., 2018. Global avian influenza outbreaks 2010-2016: A systematic review of their
distribution, avian species and virus subtype. Systematic Reviews 7: 1–12.
Cox NJ et al., 2000.Globalepidemiologyof influenza: past and present. Annual Review of Medicine 51: 407– 421.
FeareCJ, 2007. The role of wild birds in the spread of HPAI H5N1. Avian Diseases 51: 440–447.
Flint PL, 2007. Applying the scientific method when assessing the influence of migratory birds on the dispersal of
H5N1. Virology Journal 4: 132.
Fouchier RA et al., 2000. Detection of influenza A viruses from different species by PCR amplification of conserved
sequences in the matrix gene. Journal of Clinical Microbiology 38(11): 4096–101.
Fouchier RAM et al., 2005. Global task force for influenza. Nature 435(7041): 419–20.
GaidetN et al., 2008. Evidence of infection by H5N2 highly pathogenic avian influenza viruses in healthy wild
waterfowl. PLoS Pathogens 4(8): 1000127.
Gauthier-ClercM et al., 2007. Recent expansion of highly pathogenic avian influenza H5N1: a critical review. Ibis
149: 202–214.
Hall JS et al., 2015.Rapidly expanding range of highly pathogenic avian influenza viruses. Emerging Infectious
Diseases 21: 1251–1252.
Hill NJ et al., 2012. Migration strategy affects avian influenza dynamics in mallards (Anasplatyrhynchos). Molecular
Ecology 21(24): 5986–5999.
Jacobs A, 2022. Avian Flu Spread in the U.S. Worries Poultry Industry. The New York Times. Paragraph 16.
James C, 2000. Control of communicable disease manual, Washington DC: American Public Health Association.
JeongJ et al., 2014. Highly pathogenic avian influenza virus (H5N8) in domestic poultry and its relationship with
migratory birds in South Korea during 2014. Veterinary Microbiology 173: 249–257
KalthoffD et al., 2008. Highly pathogenic avian influenza virus (H5N1) in experimentally infected adult mute swans.
Emerging Infectious Diseases 14: 1267–1270.
KawaokaY et al., 1988. Is the gene pool of influenza viruses in shorebirds and gulls different from that in wild ducks.
Virology 163: 247–250.
KeawcharoenJ et al., 2008. Wild ducks as long-distance vectors of highly pathogenic avian influenza virus (H5N1).
Emerging Infectious Diseases 14: 600–607.
Kilpatrick AM et al., 2006. Predicting the global spread of H5N1 avian influenza. Proceedings of the National
Academy of Sciences, USA 103: 19368–19373
Kim JK et al., 2009. Ducks: the “Trojan horses” of H5N1 influenza. Influenza and Other Respiratory Viruses 3: 121–
128.
Koehler AV et al., 2008. Genetic evidence of intercontinental movement of avian influenza in a migratory bird: the
northern pintail (Anasacuta). Molecular Ecology 17: 4754–4762.
Krauss SD et al., 2004. Influenza A viruses of migrating wild aquatic birds in North America. Vector-Borne Zoonotic
Diseases 4: 177–189.
Lam TTY et al., 2012. Migratory flyway and geographical distance are barriers to the gene flow of influenza virus
among North American birds. Ecology Letters 15(1): 24–33.
Latorre-MargalefN et al., 2009. Effects of influenza A virus infection on migrating mallard ducks. Proceedings of the
Royal Society B: Biological Sciences 276: 1029– 1036.
Lee DH et al., 2017.Evolution, global spread, and pathogenicity of highly pathogenic avian influenza H5Nx clade
2.3.4.4. Journal of Veterinary Science 18(1): 269–280.
Lee DH et al., 2015. Intercontinental spread of Asian-origin H5N8 to North America through Beringia by migratory
birds. Journal of Virology 89(12): 6521-6524.
Lee et al., 2020. Avian Influenza, H5N8, Spreading Rapidly in Europe, What To Do About The Bird Flu. Forbes 2020.
Li KS et al., 2004. Genesis of a highly pathogenic and potentially pandemic H5N1 influenza virus in eastern Asia.
Nature 430(6996): 209–213.
Li X et al., 2014. Global and local persistence of influenza A(H5N1) virus. Emerging Infectious Diseases 20: 1287–
1295.
Liang Y et al., 2021. Novel clade 2.3.4.4b highly pathogenic avian influenza A H5N8 and H5N5 viruses in Denmark.
Viruses 13: 886.
ZOONOSIS
51
Lo FT et al., 2022. Intercontinental Spread of Eurasian Highly Pathogenic Avian Influenza A (H5N1) to Senegal.
Emerging Infectious Diseases 28: 234–237.
MarchenkoVY et al., 2011. Characterization of the H5N1 influenza virus isolated during an outbreak among wild
birds in Russia (Tuva Republic) in 2010. Molecular Genetics, Microbiology and Virology 26: 186–190.
MarchenkoVY et al., 2015. Influenza A (H5N8) virus isolation in Russia, 2014. Archives of Virology 160: 2857–2860
McLeod A et al., 2005. Economic and social impacts of avian influenza. Food and Agriculture Organization.
Merced-Morales A Pet al., 2021. Morbidity and Mortality Weekly Report Influenza Activity and Composition of the
2022-23 Influenza Vaccine-United States, 2021-22 Season 71: 2019–2020
Munster VJ et al., 2005. Mallards and highly pathogenic avian influenza ancestral viruses, northern Europe.
Emerging Infectious Diseases 11(10): 1545–51.
NormileD, 2005. Avian influenza. Are wild birds to blame? Science 310(5747): 426–428.
Olsen B et al., 2006. Global patterns of influenza A virus in wild birds. Science 312: 384–388.
Porter N, 2012. Risky zoographies: The limits of place in avian flu management. Environmental Humanities 1(1):
103–121.
Reed KD et al., 2003. Birds, migration and emerging zoonoses: West Nile virus, lyme disease, influenza A and
enteropathogens. Clinical Medicine & Research 1(1): 5–12.
SakodaY et al., 2012. Reintroduction of H5N1 highly pathogenic avian influenza virus by migratory water birds,
causing poultry outbreaks in the 2010–2011 winter season in Japan. Journal of General Virology 93: 541–550.
SalzbergSL et al., 2007. Genome analysis linking recent European and African influenza (H5N1) viruses. Emerging
Infectious Diseases 13: 713–718
SleemanJM et al., 2017. Optimization of human, animal, and environmental health by using the One Health
approach. Journal of Veterinary Science 18: 263–268.
StallknechtDE et al., 1990. Effects of Ph, temperature, and salinity on persistence of avian influenza viruses in water.
Avian Diseases 34: 412– 418.
StallknechtDE et al., 1988. Host range of avian influenza virus in free living birds. Veterinary Research
Communications 12: 125–141.
Swayne D et al., 2016. Impact of emergence of avian influenza in North America and preventative measures.
Proceedings of the Sixty-Fifth Western Poultry Disease Conference 2016.
Swayne DE et al., 2020. Influenza. In: Swayne DE, Boulianne M, Logue C, McDougald LD, Nair V, Suarez DL, editors.
Diseases of poultry; pp: 210–256.
Tian HY et al., 2015. Avian influenza H5N1 viral and bird migration networks in Asia. Proceedings of the National
Academy of Sciences of the United States of America 112: 172–177.
Uchida Y et al., 2008. Highly pathogenic avian influenza virus (H5N1) isolated from whooper swans, Japan.
Emerging Infectious Diseases 14: 1427–1429.
WallenstenA et al., 2007. Surveillance of influenza A virus in migratory waterfowl in northern Europe. Emerging
Infectious Diseases 13: 404–411.
Webster RG et al., 1992. Evolution and ecology of influenza A viruses. Microbiological Reviews 56(1): 152–179.
Webster RG et al., 2006. H5N1 influenza—continuing evolution and spread. The New England Journal of Medicine
355(21): 2174–2177.
Xu YJ et al., 2016. Southward autumn migration of waterfowl facilitates cross-continental transmission of the highly
pathogenic avian influenza H5N1 virus. Scientific Reports 6: 30262.
Zhang G et al., 2023. Bidirectional Movement of Emerging H5N8 Avian Influenza Viruses between Europe and Asia
via Migratory Birds since Early 2020. Molecular Biology and Evolution 40: 1–12
Zhang H et al., 2013. Viral and host factors required for avian H5N1 influenza A virus replication in mammalian
cells. Viruses 5: 1431–1446.
King, J., T. Harder, F.J. Conraths, M. Beer and A. Pohlmann. 2021. The genetics of highly pathogenic avian influenza
viruses of subtype H5 in Germany, 2006–2020.
