Review of Avian Influenza Outbreaks in South Korea from 1996 to 2014

Author(s): In-Pil Mo, Yeon-Ji Bae, Seung-Baek Lee, Jong-Suk Mo, Kwang-Hyun Oh, Jeong-Hwa Shin,
Hyun-Mi Kang, and Youn-Jeong Lee
Source: Avian Diseases, 60(1s):172-177.
Published By: American Association of Avian Pathologists
DOI: http://dx.doi.org/10.1637/11095-041715-Review
URL: http://www.bioone.org/doi/full/10.1637/11095-041715-Review

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AVIAN DISEASES 60:172–177, 2016

Review of Avian Influenza Outbreaks in South Korea from 1996 to 2014

In-Pil Mo,AD Yeon-Ji Bae,A Seung-Baek Lee,A Jong-Suk Mo,A Kwang-Hyun Oh,A
Jeong-Hwa Shin,B Hyun-Mi Kang,C and Youn-Jeong LeeC
A
Avian Disease Laboratory, College of Veterinary Medicine, Chungbuk National University, Cheongju, 361-763, South Korea
B
Environmental Health Research Division, National Institute of Environmental Research, Incheon, 404-708, South Korea
C
Animal and Plant Quarantine Agency, Anyang, 430-757, South Korea
Received 21 April 2015; Accepted 15 February 2016; Published ahead of print 18 February 2016

SUMMARY. Since the first outbreak of low pathogenic avian influenza (LPAI) in 1996, outbreaks of LPAI have become more
common in Korea, leading to the development of a nationwide mass vaccination program in 2007. In the case of highly pathogenic
avian influenza (HPAI), four outbreaks took place in 2003–04, 2006–07, 2008, and 2010–11; a fifth outbreak began in 2014
and was ongoing at the time of this writing. The length of the four previous outbreaks varied, ranging from 42 days (2008) to
139 days (2010–11). The number of cases reported by farmers that were subsequently confirmed as HPAI also varied, from
seven cases in 2006–07 to 53 in 2010–11. The number of farms affected by the outbreaks varied, from a low of 286 (2006–07)
with depopulation of 6,473,000 birds, to a high of 1500 farms (2008) with depopulation of 10,200,000 birds. Government
compensation for bird depopulation ranged from $253 million to $683 million in the five outbreaks. Despite the damage caused
by the five HPAI outbreaks, efficient control strategies have yet to be established. Meanwhile, the situation in the field worsens.
Analysis of the five HPAI outbreaks revealed horizontal farm-to-farm transmission as the main factor effecting major economic
losses. However, horizontal transmission could not be efficiently prevented because of insufficient transparency within the poultry
industry, especially within the duck industry, which is reluctant to report suspicious cases early. Moreover, the experiences and
expertise garnered in previous outbreaks has yet to be effectively applied to the management of new outbreaks. Considering the
magnitude of the economic damage caused by avian influenza and the increasing likelihood of its endemicity, careful and
quantitative analysis of outbreaks and the establishment of control policies are urgently needed.
RESUMEN. Revisión de los brotes de influenza aviar en Corea del Sur entre los años 1996 al 2014.
Desde el primer brote de influenza aviar de baja patogenicidad (con las siglas en inglés LPAI) en el año 1996, los brotes de influenza
aviar de baja patogenicidad se han vuelto más comunes en Corea, lo que llevó al desarrollo de un programa de vacunación masiva en
todo el país en el año 2007. Con relación a la influenza aviar altamente patógena (con las siglas en inglés HPAI), cuatro brotes tuvieron
lugar entre los años 2003-04, 2006-07, 2008 y 2010-11, respectivamente. Un quinto brote comenzó en el año 2014 y que estaba
en curso cuando se escribió esta revisión. La duración de los cuatro brotes anteriores fue variable, desde los 42 días (en el año
2008) hasta 139 días (entre los años 2010 y 2011). El número de casos notificados por los agricultores que fueron confirmados
posteriormente como altamente patógenos también varió, de siete casos entre los años 2006 al 2007 hasta 53 entre los años
2010 al 2011. El número de explotaciones afectadas por los brotes también fue variable, desde un mínimo de 286 (entre los años
2006-07) con la despoblación de 6,473,000 aves, hasta un máximo de 1,500 granjas (en el año 2008) con la despoblación
de 10,200,000 aves. Las compensaciones por parte del gobierno por la despoblación de aves fueron desde $253 millones hasta
$683 millones en los cinco brotes. A pesar de los daños causados por los cinco brotes de influenza aviar, aún no se han establecido
estrategias de control eficientes. Mientras tanto, la situación en el campo ha empeorado. El análisis de los cinco brotes de gripe
aviar reveló la transmisión horizontal de granja a granja como el principal factor que contribuyó a esta pérdidas económicas
importantes. Sin embargo, la transmisión horizontal no se pudo prevenir con eficacia debido a la falta de transparencia dentro de la
industria avícola, especialmente dentro de la industria de los patos, que se resiste a reportar casos sospechosos de manera oportuna.
Por otra parte, las experiencias y conocimientos obtenidos de los brotes anteriores aún no se ha aplicado de manera efectiva al
manejo de los nuevos brotes. Se necesitan con urgencia un análisis cuidadoso y cuantitativo de los brotes y el establecimiento de
políticas de control, que consideren la magnitud de los daños económicos causado por la influenza aviar y la creciente probabilidad
de que se convierta enzoótica.
Key words: outbreaks, duck, poultry industry, farm-to-farm transmission, economic impacts
Abbreviations: AI 5 avian influenza; AIV 5 avian influenza virus; HPAI 5 highly pathogenic avian influenza; LBM 5 live bird
markets; LPAI 5 low pathogenic avian influenza

The causative agent of avian influenza (AI) is a virus belonging
to the Orthomyxoviridae family that can be classified as highly patho-
genic AI (HPAI) or low pathogenic AI (LPAI), depending on the
severity of clinical signs. The HPAI virus serotypes currently circulat-
ing globally are related to the H5 and H7 subtypes (27). The H5
subtype was recently a subject of interest because of the potential
for transmission in humans, as evidenced by the 1997 Hong Kong
incident in which 6 of 18 human cases died (32). The H5 subtype
was also responsible for heavy economic losses in the domestic poultry
D
Corresponding author. E-mail: moip@cbu.ac.kr
industry, driven by intercontinental spread. In particular, the first
outbreak of H5N8 HPAI occurred in Korean poultry farms in 2014
and was soon followed by outbreaks in Europe and the United States,
thereby cementing the status of H5N8 as a significant global threat
(1,10,16).
Generally, the primary mode of transmission of AI virus (AIV)
occurs after horizontal transmission by wild birds traveling between
regions and countries. The secondary mode of transmission, on the
other hand, mostly occurs through contact with contaminated mate-
rials. The modes of secondary horizontal transmission are divided
into five categories (25): 1) direct exposure to AIV-infected birds;

172
 Avian influenza in Korea
2) exposure to equipment or materials contaminated with infected
respiratory secretions or feces; 3) movement of people with virus on
their shoes or clothing; 4) water contaminated by virus; and 5) dis-
semination of AIV by air. Although all of these transmission modes
play a role in HPAI outbreaks, direct exposure to infected birds is
the most important. Efficient direct exposure arises through contact
with infected birds shedding large quantities of HPAI virus into a
common environment through their respiratory secretions and feces
(26). Although the various transmission modes had been previously
identified and extensively discussed, a general lack of awareness in
the poultry industry has contributed to the ongoing horizontal trans-
mission of HPAI virus.
Although the actual mode of transmission is critical for tracing the
spread of HPAI virus among countries or regions, domestic duck
(Anas platyrhynchos) populations are also an important local source
of virus (30). The domestic duck is currently considered the most
important epidemiologic factor associated with HPAI incidence in
Korea. Although the role of domestic ducks in the propagation and
transmission of AIV is recognized, the actual threat to the poultry
industry is greater in magnitude than previously suspected.
Asia produces 88.1% of the ducks on the global market. The
top five producing countries are Taiwan, mainland China, Vietnam,
Malaysia, and Indonesia, which are also the countries with the great-
est incidence of HPAI outbreaks (9). In Korea, outbreaks of HPAI
have been frequently reported in five of the nine provinces known
for large-scale duck production. Although the duck industry was
originally a traditional business in the southern part of Korea, the des-
ignation of duck meat products as healthy by Eastern medicine led
to rapid industrialization and development in duck farming regions.
This led, in turn, to the establishment of integrated systems in the
Korean duck industry. Farms that belonged to an integrated system
frequently changed their affiliation in search of better conditions
and greater profit margins, which led to the farms linking up with
integrated companies all over the country, rather than establishing a
local supply chain. These issues with integrated systems in the duck
industry have greatly contributed to spread of AIV in Korea.
After the initial LPAI outbreak in 1996, H5N1 AIV was isolated
in duck products imported from China. Subsequent outbreaks of
HPAI included four caused by H5N1 and the current outbreak
of H5N8 (29). These outbreaks have inflicted heavy economic losses
on the country’s poultry industry. The H5N8 outbreak, which began
in 2014, became a national endemic in Korea. Despite major efforts
to control the disease, eradication of the virus was not feasible. As
new HPAI viruses are introduced to Korea by wild birds on an annual
basis, we conducted this review as an effort to assess the status of
AIV in Korea and to summarize the lessons learned from past out-
breaks to mitigate future epidemics.
LPAI outbreaks. The first outbreak of LPAI in Korea was reported
in 1996 (19). It was caused by H9N2 AI viruses and affected breeder
farms, causing mortality rates near 20% and decreasing egg produc-
tion. After the first outbreak, H9N2 AIV was found in five chicken
farms in three different regions. Mortalities ranged from 12% to
30%. All of the infected poultry were breeders, and about 100,000
chickens were ultimately destroyed (19).
Based on epidemiologic analysis, the initial stages of the outbreak
took place on poultry farms with inadequate facilities. These farms
kept birds in makeshift houses and allowed easy access to outsiders
and wild animals. All infected flocks exhibited severe drops in egg
production, mostly around 40%, although egg production ceased
completely in some cases. After the initial infection, transmission of
the virus between houses took place on a 2- to 4-day interval.
Egg production recovered within 2 wk of the first death. In general,
173
egg production recovered fully within 2 to 3 wk after the initial
LPAI outbreak. In an effort to evaluate unreported outbreaks of
LPAI that may have occurred before the 1996 outbreak, retrospective
studies were conducted to test previously collected sera for exposure
to H9 LPAI virus. All samples were negative, confirming that no
LPAI outbreaks occurred in Korea before 1996 (19).
After the first outbreak of LPAI in 1996, nationwide serologic sur-
veys were conducted on poultry farms to screen for AIV infection. No
evidence of infection with H9N2 or any other AIV serotype was
found. However, in 1999, two farms in the Gyeong-gi province
were confirmed to be infected with the H9N2 subtype LPAI virus.
Birds exhibited reduced egg production and increased egg laying
and mortality. By 2000, LPAI had spread across the entire country
and national serologic surveys were again conducted. Nearly 50% of
layer farms were confirmed positive for the H9N2 subtype, which
led to the development of government policies to implement large-
scale vaccination programs. Mass vaccination against H9N2 LPAI
was then initiated in 2007. After the implementation of national vac-
cination programs, H9N2 LPAI outbreaks became nearly nonexistent
on chicken farms, although other LPAI subtypes, such as H3N2 and
H6N1 were consistently isolated from ducks, geese, and Korean
native chickens on small-scale farms. The H9N2 subtype has also
been isolated on some occasions. A number of subtypes continue to
be frequently isolated, especially from live bird markets (LBM) and
small-scale, backyard bird productions. Notably, LBMs are thought
to play an important epidemiologic role in the dissemination of
AIV (17,23). Active surveillance of Korean LBMs has shown that
the H9N2 LPAI virus has become more genetically diverse through
genetic reassortment with AIV strains found in aquatic birds
(7,14,20).
H5N1 subtype HPAI outbreaks. The first detection of HPAI virus
in Korea was confirmed in 2000 by isolation of HPAI virus from
duck meat imported from mainland China. The virus was identified
as the H5N1 subtype (29). An embargo was placed on imported
Chinese meats, and 4588 tons of meat were destroyed. A survey
was conducted of 11 Chinese processing plants that were exporting
products to Korea, and two cases of HPAI and three cases of velogenic
Newcastle disease were discovered. Since 2000, five HPAI outbreaks
have taken place in Korea (Table 1).
The first HPAI outbreak (2003–04) began at a layer farm on
December 10, 2003. It lasted 102 days and affected 10 different
regions (2,31). Of 49 reported cases, 19 were confirmed positive for
HPAI virus: 10 originating from chicken farms and 9 from duck
farms. Other farms were confirmed positive by active surveillance.
At the end of the outbreak, 5,285,000 birds on 392 farms were
depopulated, and $458 million was spent in reimbursement. During
this first HPAI outbreak, the possible role of migratory birds in virus
dispersal was suggested, although the exact mechanism was not eluci-
dated. The likelihood of direct viral transmission from infected birds
was low, while that of indirect contact with vehicles or equipment
contaminated with HPAI virus was both high and critical for horizon-
tal transmission. Indeed, the first incident of HPAI was reported on a
layer farm, while epidemiologic studies confirmed that a nearby duck
parent stock farm was the source of infection (2).
The second HPAI outbreak (2006–07) began on November 22,
2006, with a report filed by a layer farm (3,15). The outbreak lasted
104 days and spread to five regions. A total of 24 cases were reported,
with 7 confirmed positive by virus isolation. Positive farms included
four chicken farms, two duck farms, and one quail farm. Active
surveillance identified another 5 positive farms, bringing the total
to 12. As a result of the outbreak, 2,800,000 birds on 460 farms
were destroyed, and $253 million was paid in compensation. In this
174 I.-P. Mo et al.

Table 1. Summary of HPAI (H5N1 and H5N8) outbreaks reported by the poultry industry in Korea from 2003 to 2014.
Outbreaks
2003–04 2006–07 2008 2010–11 2014–15A
Cases
First reported Dec. 10, 2003 Nov. 22, 2006 Apr. 1, 2008 Dec. 29, 2010 Jan. 16, 2014
Duration (days) 102 104 42 139 431
Regions involved 10 5 19 25 53
PositivesB 19/49 (38.8) 7/24 (29.2) 33/68 (48.5) 53/103 (51.5) 37/43 (86.0)
Chicken 10 4 21 18 15
Duck 9 2 6 33 21
Others 0 1 6 1 1
Compensation (millions of dollars) 458 253 683 670 Ongoing
Depopulation
Farms 392 460 1500 286 707
Birds (6103) 5285 2800 10,200 6473 17,923
A
From Jan. 16, 2014 to Mar. 22, 2015.
B
Number of positive cases/number of reported cases (positivity rate).

outbreak, the HPAI virus was isolated from migratory bird feces, and
antibodies were detected in wild birds. Possible means of farm-to-
farm transmission included movement of birds (infected or contami-
nated), people, vehicles, and equipment. However, there was no
evidence of direct transmission from wild birds or by related means,
such as the movement of people or vehicles contaminated with wild
bird feces. Based on the genetic sequences of isolated viruses and their
geographic locations, there were two separate introductions during
this outbreak (3,15).
The third HPAI outbreak (2008) started on April 1, 2008,
according to a report filed by a layer farm. During the 42 days of
the outbreak (4,13), 68 cases were reported from 19 different regions:
33 cases were confirmed as positive for HPAI virus. Positive farms
included 21 chicken farms, 6 duck farms, and 6 farms breeding other
birds, such as Korean native chickens, quails, or wild ducks. Active
surveillance identified another 73 farms, bringing the total number
of positive farms to 106. After the outbreak, 10,200,000 birds on
1500 farms had been destroyed, and $683 million paid in reimburse-
ment. This outbreak differed from the previous two outbreaks in
many respects. The rate of transmission was notably high, and the
outbreak occurred in the spring. The mortality of ducks was also
very high. The most interesting characteristic of this outbreak was
the involvement of small-scale dealers whose job was to deliver
live birds to garden-style restaurants, LBMs, and small farms. This
demonstrates that even minor distribution routes can play a key role
in the dispersal of virus. Two specific routes of transmission were iden-
tified. The first route, responsible for 70% of the outbreak, was the
common route that involves feed trucks, distributors, and mass poul-
try shipping. The second route involved contaminated poultry bought
from traditional LBMs and minor dealers. This route brought the
virus into urban areas and accounted for 30% of the outbreak.
The fourth HPAI outbreak (2010–11) started on December 29,
2010, according to a report from a layer farm. The outbreak lasted
139 days and affected 25 regions (5,12). There were 103 cases
reported, with 53 confirmed positive for HPAI virus. Positive farms
included 18 chicken farms, 33 duck farms, and 1 pheasant farm.
Active surveillance detected another 38 positive farms, bringing the
total number of infected farms to 91. By the end of the outbreak,
6,473,000 birds had been destroyed on 186 farms, and $670 million
paid in compensation. This outbreak was the longest (139 days) and
largest in terms of the number of reported cases. The number of
reports of suspected HPAI was also greatest during this fourth out-
break. Of the 53 confirmed cases, 33 involved ducks, indicating
significant levels of AIV infection in these birds.
The current H5N8 subtype HPAI outbreak. The fifth (and ongo-
ing) HPAI outbreak started on January 16, 2014, and
43 cases had been reported through March 22, 2015 (16,18).
Of the 43 reported cases, 37 were confirmed as positive for H5N8. Pos-
itive farms include 15 chicken farms, 21 duck farms, and 1
Korean native fowl farm. Active surveillance detected 254 positive
farms. An additional 66 farms were confirmed positive according to
cases submitted to the Animal and Plant Quarantine Agency of Repub-
lic of Korea (Anyang, Korea) for diagnosis At the last count, 357 farms
were confirmed positive for H5N8. With 58 cases of infected wild
birds, there were 415 positive cases. At the time this review was being
finalized, 17,923,000 birds on 700 farms had been destroyed. The
amount spent in compensation is not currently available (Tables 1, 2)
Surveys were conducted by tagging infected premises as the point
of origin and designating a specific declared area. All farms included
in this area, or farms epidemiologically linked to suspected or HPAI-
positive premises, were subjected to the survey. Nationwide surveil-
lance was also conducted in regions where farms were located near
wild bird habitats. This involved collecting and analyzing fecal sam-
ples. Although the surveillance program provided important informa-
tion, including virus and antibody monitoring data collected from
wild birds (18), analysis was excluded from this study because of the
amount of data. Therefore, the current study only includes survey
results from infected farms, farms within the designated area, and
farms considered to be epidemiologically linked to infected farms
(Table 2).
The significance of HPAI outbreaks in Korea. Starting at the
beginning of the 21st century, the Korean duck industry expanded
rapidly. One million ducks were bred in 1991, and seven million in
2000. After the introduction of national statistical surveys, the total
number of birds grew steeply, reaching 15 million birds by the second
quarter of 2011. This dramatic increase from 7 million ducks in 2000
to 15 million in 2015 was probably a result of improved estimation
methods. After reaching its peak of 15 million birds, the population
decreased to an average of 11 million birds per year. The duck popu-
lation through January 2013 (prior to the H5N8 outbreak) was
10,890,000 birds; only 7.9% of the total number of chickens in
the country (Fig. 1). However, after the 2003 HPAI outbreak, the
proportion of HPAI-positive duck cases increased steeply to 62.2%
during the fourth outbreak in 2010. During the fifth outbreak,
56.5% of all positive cases were ducks. This indicates that HPAI
incidence was 9.7 times higher in ducks than in chickens.
The number of self-reported HPAI-positive farms was compared
with the number of farms confirmed by epidemiologic studies (Fig. 2).
 Avian influenza in Korea 175

2398 (100)
43 (100)
1200 (100)
152 (100)
1003 (100)
Total
6 (14.0)
418 (100) 254 (21.2) 946 (78.8)
86 (56.6)
945 (94.2)
793 (100) 415 (17.3) 1983 (82.7)
2014–15
Negative
103 (100) 37 (86.0)

123 (100) 66 (43.4)

149 (100) 58 (5.8)
Positive
Total

Cases include both live and dead wild birds that were sampled by the surveillance team excluding fecal samples collected from wild bird habitats.
50 (48.5)
380 (90.9)

129 (86.6)
682 (86.0)

Fig. 1. The population of chicken and duck between June 2011 and
123 (100)
Negative
2010–11

December 2014 in Korea.

The number of reports of HPAI-positive farms increased steadily each

year, with the exception of 2014. The positivity rate of all reported
(100) 53 (51.5)

20 (13.4)
(100) 111 (14.0)
(100) 38 (9.1)
Positive

farms decreased across the four outbreaks that took place between
0 (0)

2003 and 2010 (from 73.7%–58.3% to 40.0%–47.7%). Even as

the positivity rate for reported farms decreased, the positivity rate for
(100)

farms confirmed by epidemiologic studies increased to 91.1%. This

(0)

suggests a decrease in reporting by farm owners and is supported by

Total
14 (28.6) 35 (71.4) 49 (100) 7 (29.1) 17 (70.9) 24 (100) 42 (61.8) 26 (38.2) 68
5 (100) 5 (2.2) 223 (97.8) 228 (100) 55 (4.7) 1127 (95.3) 1182
8 (2.1) 371 (97.9) 379
264 (100) 264
20 (12.2) 136 (87.8) 156 (100) 12 (1.6) 746 (98.4) 758 (100) 105 (5.4) 1788 (94.5) 1893

the observation that many farms near to reporting farms turned out
to be positive in epidemiologic surveys.
Outbreaks
Comparison of positive HPAI cases from different sources across five outbreaks (2003 to 2014).

The positivity rate for reported farms was higher in 2014 than in
Negative
2008

the previous four outbreaks. The positivity rate was between 28.6%
and 61.8% but jumped to 86% in 2014 when 37 of 43 reported cases
were confirmed to be HPAI positive (Table 2). Although various fac-
tors may be responsible for the increase, the most likely explanation
Positive

0 (0)

is that farm owners were reluctant to file a report until the damage
Cases were submitted for routine diagnosis of poultry diseases at government facilities.

grew to such a level that they were forced to report the incident as a
last resort. This explanation is supported by the observation that
Cases include epidemiologically linked farms and farms within the designated area.
506 (100) 506 (100)

254 farms near to or epidemiologically linked with self-reported

Total

NR

farms turned out to be positive for HPAI.

Three types of surveys were conducted on wild birds to monitor
HPAI: examination of dead birds, examination of live birds captured
2006–07

by surveillance teams, and diagnostic testing of fecal samples collected

Negative

NR

from the field. The data in Table 2 are derived from live and dead
birds. Examination of wild birds was initiated in 2003. A large-scale
effort was made in 2008, but all samples were negative; however,
Positive

99 (99.0) 100 (100) 0 (0)

2 (100) NRE

Cases reported by the farmer or stakeholders.

Total

2 (40.0)
2003–04
Negative

0 (0)
B

3 (60.0)
2 (100)
Positive

NR 5 not reported.
1 (1.0)

Number (%).
SurveillanceC

Wild birdsF
DiagnosisD
Table 2.

A
Cases
Reported

Total

Fig. 2. HPAI positivity rate on farms reported by the poultry

D
C
A
B

E
F

industry or identified by government surveillance.

176 I.-P. Mo et al.
positive samples were collected during subsequent outbreaks (20 in
2010 and 58 in 2014). This indicates a trend of increasing infection
rates in wild birds (Table 2).
In the event of an HPAI report, monitoring programs are being
mobilized to survey neighboring farms and specific regions of the
country, such as those densely populated with duck breeding farms.
The number of positive cases confirmed by HPAI monitoring pro-
grams increased each year, with five cases in 2003, 1182 in 2008,
and 1134 cases 2014. With the exception of 2003, the positivity
rate from epidemiologic studies also increased each year, from 2.2%
in 2006, 4.7% in 2008, and 9.1% in 2010, to 21.2% in 2014, which
was the year with the highest rate (Table 2).
DISCUSSION
Since the first outbreak of LPAI in 1996, the situation regarding AI
in Korea has worsened. This is reflected by the progression of HPAI
outbreaks, which began in 2003 after the first isolation of an HPAI
virus from duck meat imported from mainland China in 2000
(12,13,15,16,31). Although there have yet to be any human cases,
the virus is now endemic in Korea. Despite the mobilization of con-
siderable resources and manpower to curtail the virus spread, the virus
was not eradicated, and sporadic outbreaks continue to this day (11).
The worst-case scenario for the Korean poultry industry is the spill-
over of AIV to humans. Most previous cases of human deaths caused
by H5N1 virus infections occurred after direct contact with contami-
nants (28). An endemic HPAI virus could, therefore, transmit to farm
personnel (24). The chicken industry modernized and industrialized
20 yr ago. By contrast, the duck industry is still relatively new. As
such, the quality of facilities and the overall level of biosecurity are
still insufficient to mitigate the risk of AIV spread.
The Korean duck industry has undergone rapid industrialization
over the past 10 yr due to increased demand for duck meat (Fig. 1).
One example of this industrialization is the introduction of the
vertical integration system, wherein individual farms affiliate with
an integrated company. Currently, 95% of all Korean duck farms
are affiliated. There are 14 active integrated companies in Korea,
most of which center on duck processing plants. Competition between
companies has led to the aggressive integration of duck farms. More-
over, individual farms frequently change their affiliations, regardless
of region, to ensure the greatest profit. Thus, rather than handling
only ducks from farms within a given region, plants process animals
originating from farms that are spread all over the country. For this
reason, ducks are frequently transported nationwide, greatly facilitat-
ing the spread of HPAI virus (8,24). Information on the daily
transport of chicks and market-aged ducks is only available to the
companies, which hinders early virus detection because authorities
can only identify virus after an outbreak or through an epidemiologic
study conducted in response to a report of a suspected case. Although
clinical examinations and laboratory tests, such as real-time PCR, are
being used to monitor market-aged ducks, their actual effectiveness in
terms of virus surveillance has yet to be determined.
Because of the rapid development of the Korean duck industry, the
quality and sophistication of farm facilities, farm management, and
hygiene and biosecurity measures are poor compared with those in
the chicken industry. Most duck farms are not isolated from the
external environment. Duck houses are commonly exposed to wild
birds, mice, and humans, all of which can be a source of pathogens,
severely hampering efforts to control the virus (8). The rural areas
of Korea tend to be very socially interconnected. Once a member of
a family starts a duck farm, many relatives also begin to breed ducks,
resulting in high densities of ducks in a given area. As in other
countries, the movement of family members and their equipment
in vehicles (all potentially contaminated with the virus) is an impor-
tant mode of HPAI virus spread (21). The social bond between family
members is also an important epidemiologic factor, as whole families
may decide to delay reporting suspected HPAI cases. For these
reasons, the positivity rate of farms socially and epidemiologically
connected to a reporting farm is often very high (Table 2; Fig. 2).
In Korea, most of the first HPAI (H5N1) incidence reports were
made by chicken farms because chickens experience higher mortality
than ducks and manifest particular necropsy findings that are unique
to HPAI. The H5N8 HPAI virus responsible for the 2014 outbreak
has a slower transmission rate and a longer course of development
than the H5N1 viruses but causes the same characteristic lesions in
chickens (6,11). This can lead to misdiagnosis of the disease as fowl
typhoid. In one specific case, a college veterinary laboratory con-
firmed HPAI in a chicken previously diagnosed with fowl typhoid
by the farm owner (6). The unique characteristics of H5N8 may
delay or prevent reporting of suspected cases, thereby complicating
its control. As layers or breeders are reared for 68 to 85 wk before
being processed in a plant, they could make a disproportionately
high contribution to transmission when compared with short-lived
broilers and ducks. Although Korea has laws that require reporting
when over 5% mortality occurs, the effectiveness of the system has
not been fully verified.
The efficient control and prevention of HPAI requires provision of
high-level veterinary services. Countries that have experienced HPAI
epidemics generally lack sufficient funding and technology to support
veterinary medicine (8,22). Despite the relatively high quality of vet-
erinary services and the availability of adequate budgets, HPAI out-
breaks have taken place every 2–3 yr in Korea since 2003. The
rapid application of veterinary expertise is necessary during the early
stages of an outbreak to prevent nationwide horizontal transmission.
Currently, the Animal and Plant Quarantine Agency is the most
experienced government agency that deals with disease outbreaks,
but its jurisdiction does not extend to the national level because it
lacks the administrative authority to manage national biosecurity pol-
icies. Also, the bureaucrats involved in high-level decision-making at
the Ministry of Agriculture, Food, and Rural Affairs tend to serve
for only 1 to 2 yr before being transferred to another position, so
they usually have no experience of handling HPAI outbreaks. This
lack of experience contributes to the inconsistency of policies related
to HPAI management and impedes implementation of appropriate
and effective intervention measures (22).
This assessment of the five HPAI outbreaks that have taken place
in Korea highlights several important points relevant for controlling
future transmission. In particular, there is a great need to establish
an animal health system that retains the knowledge and experience
earned from prior outbreaks to guide future actions. This report pro-
vides insight that may guide the development of polices in countries
(such as Korea) in which HPAI viruses are endemic and in which
the available funds and technology are sufficient to ensure implemen-
tation of effective interventions.
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ACKNOWLEDGMENT
This research was supported by a grant from the Animal and Plant
Quarantine Agency of Republic of Korea (Z-1543084-2013-15-03).