|
Global Avian Influenza Surveillance
And
Pandemic Preparedness
Joseph P. Dudley
Department of Earth Science, The University of Alaska Museum
Institute of Arctic Biology-University of Alaska Fairbanks
Science Applications International Corporation (SAIC)
Introduction
During first six months immediately following the release of the
U.S. National Strategy for Pandemic Influenza (White House, 2005),
the number of countries with confirmed outbreaks of the highly pathogenic
H5N1 avian influenza virus in birds increased from 16 countries
to 55 countries, and the number of countries with confirmed fatal
human bird flu cases increased over this same period from only five
countries in Asia to a total of at least 10 countries in Asia, Africa,
and the Middle East.
Although the first known human cases of H5N1 avian influenza
(“bird flu”) were recorded in Hong Kong during 1997, the current
bird flu epizootic is generally cited as having begun in 2003
and can be benchmarked to confirmed fatal human bird flu cases
that occurred in China during February and November 2003, and
in Vietnam during October-December 2003. H5N1 outbreaks began
on commercial poultry farms in Indonesia and Thailand during the
period between August-November 2003, and in Cambodia and Korea
during December 2003. As of 31 July 2006, Asian H5N1 virus infections
have reportedly been confirmed from at least 118 species of birds
and 16 species of mammals from 58 countries in Asia, Africa, and
Europe. Confirmed human mortality from the H5N1 bird flu virus
has been reported from China (1997, 2003), Thailand (2004), Cambodia
(2005), Indonesia (2005), Turkey (2006), Iraq (2006), Egypt (2006),
Azerbaijan (2006), and Djibouti (2006). A total of at least 257
confirmed human bird flu cases, including 139 fatalities, have
been reported worldwide for the period between 1 February 2003
and 31 July 2006 (Table 1).
The sequence and timing of events that have unfolded over the
course of the H5N1 epizootic during the period between January
2003 and July 2006 have demonstrated repeatedly that potential
suspected outbreaks in poultry or wild birds may not be reported
by farmers or local officials because of economic concerns, and
that even when reported, such outbreaks may not investigated in
a timely fashion by agriculture or public health officials due
to reluctance to reveal the existence of potential outbreaks or
a lack of technical capacity to perform a thorough investigation.
Even in those cases where outbreaks have been investigated and
confirmed, the reporting of laboratory confirmations of H5N1 cases
in birds or human by governments and
|
multilateral organizations may
be delayed or suppressed entirely for policy or economic reasons,
or -- in the case of public sector and private sector scientists
and institutions -- for reasons of data control and publication
priority.
We must increase the effectiveness and transparency of global surveillance
networks for the H5N1 bird flu virus and other dangerous pathogens
that can infect animals and humans (Dudley 2004a). Pandemic preparedness
and response programs for diseases like the H5N1 bird flu that can
infect animals as well as humans must integrate and coordinate human
disease surveillance with monitoring and testing of pathogens in
wildlife, food animals, farm animals, and household pets. We must
greatly reduce the time required to detect and diagnose H5N1 bird
flu infections in birds and humans, and increase our capability
to monitor the potential mechanisms by which pathogens that infect
people as well as animals can be transported through domestic and
international trade and transportation networks. We need to increase
public understanding of the level and degree of biosecurity and
public health threats presented by avian influenza viruses and other
human-transmittable animal diseases, and to increase the capacity
of countries worldwide to prevent, detect, diagnose, and contain
disease outbreaks in avian, animal and human populations (Dudley
2004a).
There is increasing scientific and public concern regarding the
continued expansion and proliferation of the lethal human-transmissible
and highly pathogenic H5N1 avian influenza virus ("bird flu")
across Eurasia and Africa, and the perceived potential for the
H5N1 Asian bird flu strain to evolve into a pandemic human influenza
virus that could spread worldwide and undermine the public heath
security and economic vitality of countries all over the globe
(Guan et al 2004, Webster et al 2006). This factor is of definite
concern because of the demonstrated high rate of change in H5N1
virus strains circulating in China and southeast Asia during the
past decade which have increased the environmental stability of
the virus outside of host organisms, and increased the lethality
and infectiousness of the Asian H5N1 bird flu virus in birds,
humans, and other mammals. Although most human cases have been
linked to contact with infected poultry or birds, probable or
suspected instances of human-to-human transmission of H5N1 bird
flu have been reported to date from Thailand, Hong Kong, |
| Vietnam, and Indonesia (Ungchusak 2005, Parry
2004, Yeung & Wong 2005, WHO 2004, Seyaningseh 2006, Butler
2006).
The greatest current threat from a pandemic preparedness perspective
is that the H5N1 bird flu will mutate into a pandemic human influenza
virus with SARS-like human epidemic potential that could spread
worldwide with public health and economic impacts paralleling
or surpassing those seen in the global "Spanish Flu"
epidemic of 1918-1919. China and southeastern Asia have a long
history of continuous occupation by humans having concurrent intimate
association with wild and domesticated ducks and geese (natural
hosts of H5N1 avian influenza viruses), and wild and domesticated
swine through intensive hunting and animal husbandry. Recent experiences
with at least three important emerging lethal pathogens that can
be transmitted between and among humans, wildlife, and domesticated
animals -- e.g., the highly pathogenic Asian H5N1 avian influenza
virus, the SARS virus, the Nipah virus –- demonstrate the critical
importance of southeastern Asia as a source and reservoir for
emerging viral diseases that could have severe global public heath
impacts (Dudley 2004b).
There is a significant risk that the H5N1 virus could mutate
into a pandemic flu strain, given the already extensive changes
that have been documented in the virulence and epidemiological
characteristics of the H5N1 viruses circulating in southeast Asia
during the past decade. Experimental and empirical studies have
shown that H5N1 avian influenza strains in circulation in Southeast
Asia since 2001 are significantly more virulent to birds, humans
and other species of mammals than earlier strains, and that H5N1
outbreaks in poultry, wild birds, and humans exhibit different
epidemiological characteristics than precursor H5N1 strains recovered
from outbreaks in Asia between 1997 and 2001 (Webster et al 2006,
de Jong & Hien 2006). The unusually large number of domesticated
ducks dying from bird flu in southern China indicates H5N1 virus
circulating in China since 2002 have been significantly more virulent
than H5N1 strains encountered in previous years, particularly
so because both wild and domesticated ducks are usually considered
asymptomatic carriers of H5 influenza strains (Sturm-Ramirez et
al 2004). Experimental studies have demonstrated that certain
H5N1 strains circulating in Southeast Asia during 2003 and 2004
were significantly more virulent in birds and mammals than strains
collected in previous years (Li et al 2004, de Jong & Hien
2006). Research studies have indicated that vaccinated chickens
may be able to serve as active carriers and vectors for the H5N1
bird flu virus, a phenomenon that would allow both vaccinated
chickens and domesticated ducks to serve as cryptic carriers and
asymptomatic reservoirs for the H5N1 bird flu virus (Chen et al
2006, Webster et al 2006).
The first evidence of the human disease threat associated with
the current 2003-2005 H5N1 epizootic came from a family disease
cluster confirmed in China during February 2003 that included
two confirmed cases (one fatal, one non-fatal) and another possible
fatal case in an untested individual who died of severe respiratory
symptoms (Edwards et al 2004, Peiris et al 2004). The first reported
confirmed human fatalities associated with the current H5N1 epizootic
in Southeast Asia in China during February 2003 were |
followed by confirmed human
mortality in Vietnam during October and November 2003), another
fatal case in China during November 2003 (Zhu et al 2006). Subsequently,
fatal human cases were reported from Thailand (January 2004), Cambodia
(January 2005), Indonesia (July 2005), Turkey (January 2006), Iraq
(February 2006), Azerbaijan (March 2006), Egypt (March 2006), and
Djibouti (May 2006). The official tally of confirmed human cases
for the current ongoing H5N1 epizootic published by WHO does not
include at least three reported confirmed human cases (including
two fatal) that occurred in China during 2003 (Edwards et al 2004,
Peiris et al 2004, Zhu et al 2006).
Although most confirmed human H5N1 cases have been attributed
to H5N1 virus transmitted to humans through contact with domesticated
poultry, principally chickens or ducks, through contact with live
birds or the ingestion of uncooked poultry tissues (e.g., raw
ducks blood, raw duck liver), and there have been fatalities in
Azerbaijan linked to contact with dead wild swans. There are other
potentially significant risk factors tied to environmental exposure
and contamination. The use of poultry manure in aquaculture was
identified twenty years ago as a significant risk factor in the
evolution of pandemic influenza viruses (Scholtissek & Naylor
1988). The widespread use of poultry manure as a fertilizer for
fish farming and aquaculture, when coupled with evidence that
asymptomatic vaccinated chickens as well as domestic ducks can
carry and shed the H5N1 virus without exhibiting clinical disease
symptoms (Webster et al 2006, Chen et al 2006), greatly increases
the risk of spill-over infections of migratory birds from unprocessed
poultry manure used in aquaculture operations or direct human
infections acquired from fish or water contaminated with H5N1
virus from poultry manure. Dead poultry and poultry offal from
slaughterhouses used in fish farms to feed some fish species raised
for human consumption (e.g., catfish, snakeheads) constitute an
additional source for possible environmental contamination or
human infection through aquaculture industry produce and supply
chains. The widespread practice among farmers of feeding dead
poultry unfit for sale or human consumption to pigs, and the possibility
of exposure for free-ranging village pigs through eating sick
or dead poultry or wild birds infected with the H5N1 virus, increases
the risk that the H5N1 strain could recombine with a swine or
human virus and mutate into a dangerous pandemic flu strain (Ito
et al 1998).
The epidemiological and public health significance of confirmed
fatal asymptomatic and atypical human infections with the H5N1
bird flu virus are a serious concern that has received remarkably
little attention from the World Health Organization and public
heath authorities. Confirmed fatal asymptomatic bird flu cases
include two elderly people in Vietnam who were apparently tested
because they were close relatives of other confirmed victims of
the H5N1 virus (Anonymous 2005), and a non-fatal case in an elderly
male member of another family bird flu cluster in Hanoi, Vietnam
that may has been linked to possible human-to-human transmission.
The discovery of “atypical” fatal H5N1 infections associated with
encephalitis or gastroenteritis syndromes in Thailand and Vietnam
may be of critical importance because of the high prevalence of
mortality in Southeast Asia of other much more common diseases
that exhibit similar disease |
symptoms, including Japanese encephalitis,
amoebic dysentery, dengue fever, and cholera (de Jong et al 2005,
Apisarnthanarak 2004, Areechokchai 2006).
Discussion
Chronicle And Commentary
The origin of current pandemic of the highly pathogenic H5N1
avian influenza virus in the southeast Asia/Pacific region can
be traced to outbreaks of highly pathogenic H5N1 virus circulating
within poultry populations in southeastern China since 1996, which
caused an outbreak in Hong Kong during 1997 that killed six of
the 18 people known to have been infected by the virus (Peiris
et al 2004). Although the 1997 outbreak was apparently successfully
suppressed in Hong Kong through wholesale culling and the closing
and disinfection of poultry markets and poultry farms and other
measures, highly pathogenic H5N1 viruses continued to circulate
among ducks, geese and other domesticated poultry in mainland
China (Webster et al 2002, Sturm-Ramirez et al 2004). Current
evidence indicates that H5N1 avian influenza viruses have now
become endemic in domesticated duck and poultry populations in
many areas of southeastern Asia and Indonesia (Dudley 2004b, Li
et al 2004), and may not be eradicable or even controllable in
some areas of Asia and Africa during the foreseeable future.
My analysis of the available information indicates that the spread
of the H5N1 bird flu from Asia into the Middle East, Eastern Europe,
has been mediated largely by movements of infected poultry or
contaminated poultry equipment/supplies through international
trade networks. Research showing that vaccinated chickens may
carry the H5N1 as serve as asymptomatic reservoirs and vectors
for the H5N1 virus suggests that international trade in asymptomatic
vaccinated chickens or day-old chicks may have been responsible
for the transcontinental spread of the H5N1 virus through the
international poultry supply chain into commercial poultry flocks
in countries in such as Nigeria, Russia, Turkey, and the Ukraine.
Illegally-imported infected domesticated poultry has been identified
by Nigerian government officials as a probable source for the
introduction of the Asian H5N1 avian influenza virus to Nigeria,
and the international trade in captive wild bird species has been
responsible for the introduction of H5N1-infected birds to Taiwan,
Belgium, and the United Kingdom (Ducatez et al 2006, Dudley 2006).
The extensive and often poorly regulated global trade in live
wild bird species for the exotic pet and falconry trade includes
hundreds of species of birds, large and small (ratites, songbirds,
parrots, raptors, doves, pheasants), and the Asian H5N1 virus
has been confirmed from other exotic bird species originating
from legal or illegal international trade networks in the United
Kingdom, Belgium, and Taiwan. The exotic bird trade in the European
Union alone is estimated at two million birds annually, while
the total global trade has been estimated to be as high as six
million to ten million birds annually that generates revenues
estimated at US$2-4 billion annually. During October 2005, the
H5N1 virus was confirmed from three of 19 species of birds in
a consignment of more than 1037 exotic birds intercepted by customs
officials while being smuggled by ship from China to Taiwan, |
and an H5N1 outbreak was confirmed in the
United Kingdom among birds imported from Taiwan and South America
through international pet trade networks (Dudley 2006).
Migratory birds and waterfowl have been cited as the possible
cause of H5N1 outbreaks among poultry in Korea (2003), Japan (2004),
Thailand (2004), Russia (2005), Kazakhstan (2005), Romania (2005),
Ukraine (2005), Croatia (2005), and Turkey (2005) (Liu et al 2005,
Dudley 2006, Chen et al 2006) . Although waterfowl (ducks, geese)
and other water-associated bird species (storks, gulls, cormorants,
sandpipers, coots, grebes) are cited as natural hosts and reservoirs
for H5N1 avian influenza viruses, many experts believe that the
highly lethal, human-transmissible Asian H5N1 virus strains now
in circulation did not emerge from wild waterfowl, but evolved
in -- and subsequently emerged from – domesticated poultry populations
in China and southeast Asia (Li et al 2004, Chen et al 2006).
Genetic studies have shown that certain important virulence factors
in the current lethal human-transmissible Asian H5N1 virus originated
in southern China from the acquisition of genes from an H9N2 avian
influenza virus circulating in domesticated quail by a H5N1 virus
strain present in domestic geese (Webster et al 2002). Subsequent
genetic studies have shown that the H5N1 viruses circulating in
Indonesia are derived from a strain detected in Yunnan, China
during early 2003 (Li et al 2004).
H5N1 virus was recovered from a dead whooper swan (Cygnus cygnus)
at Erhel Lake, Mongolia (Fig. 1), and at least five different
species of swans have been confirmed with H5N1 infections. Wild
swans have been implicated in the dispersal of the H5N1 virus
during the winter of 2006 into southern and eastern Europe from
countries in the Black Sea region (Ukraine, Turkey, Romania) where
H5N1 outbreaks in poultry have been observed since September-October
2005. Wild swans infected with H5N1 virus have been reported from
Austria, Azerbaijan, Bosnia, Bulgaria, Croatia, Czech Republic,
France, Georgia, Greece, Germany, Hungary, Iran, Italy, Mongolia,
Poland, Romania, Russia, Serbia, Slovenia, Slovakia, and the United
Kingdom. As noted elsewhere in this paper, at least four human
deaths from H5N1 acquired through contact with dead wild swans
were recorded in Azerbaijan (Gilsdorf et al 2006).
The demonstrated ability of domesticated ducks and vaccinated
chickens to serve as cryptic carriers of the Asian H5N1 bird flu
virus, and the confirmation of H5N1 infections from at least ten
species of birds marketed through international exotic animal
trade networks, demonstrates the high risk for the international
and transcontinental importation of the H5N1 through legal or
illegal imports of poultry or live exotic bird species. While
further dispersal of the H5N1 through wild bird species probably
cannot be avoided, increased efforts should be made to help prevent
the further unnecessary proliferation of the Asian H5N1 bird flu
through the commercial trade and supply chain networks.
The Numbers Game
It is important to recognize that the total number of bird flu
outbreaks among both animals and humans is undoubtedly much higher
than data on |
| validated laboratory-confirmed cases published
by the World Animal Health Organization (OIE) and World Heath Organization
(WHO) indicate, given that the H5N1 virus has been circulating widely
for several years in remote rural areas of Southeast Asia and Indonesia
where veterinary and medical services are either rudimentary or
non-existent, and within countries where epidemiological data on
human and animal diseases are unavailable, inaccurate, unreported,
or actively suppressed by officials at the local, provincial or
national levels. The official statistics from the OIE are limited
to H5N1 outbreaks in poultry or wild birds officially confirmed
and reported by government agencies, a process shown to be subject
to errors of both omission [i.e., failure to report confirmed outbreaks]
and commission [i.e., submission of false pathogen identification
reports], while WHO statistics on the incidence human H5N1 data
are undoubtedly underestimates because of the limited data available
on possible human outbreaks in remote rural areas of most Asian
and African countries affected by H5N1 outbreaks where people have
little or no access to medical doctors or public health services.
Even under the best of circumstances, the process of actually
confirming and reporting outbreaks of H5N1 or other pathogens
of potential high agricultural or public health impacts may involve
protracted delays even in countries such as the United Kingdom
that have highly developed animal and human pathogen testing infrastructures,
which maintains the European Union’s international reference laboratories
for avian influenza. An H5N1 outbreak in a captive bird quarantine
facility in the UK during October 2006 went undetected for a period
of at least three weeks, and it took a reported total of eight
days for authorities in the United Kingdom to collect and confirm
H5N1 virus from a dead swan discovered in the city of Fife, Scotland
in March 2006 (Dudley 2006).
The observed lack of transparency and cooperation within and
among many of the governments, international organizations, multilateral
agencies, laboratories, and individuals involved with the surveillance,
diagnosis, and reporting of bird flu in animal or human populations
has been -- and continues to be –- a nearly insurmountable impediment
to the effective control and eradication of the Asian bird flu
virus and a risk factor that is frequently overlooked in pandemic
preparedness planning processes. The national governments of China,
Indonesia, and Thailand are known to have suppressed the public
reporting of suspected and confirmed outbreaks of H5N1 in poultry
in the past, but this problem is by no means restricted to only
these three countries. Government authorities in Japan delayed
ten months before reporting the detection of five non-fatal human
cases of H5N1 cases among poultry workers and culling personnel
infected during a February 2004 in Kyoto. During July 2006, the
government of Thailand was suppressing the reporting of confirmed
new H5N1 outbreaks in humans and poultry at the very same time
that the country was hosting a US-funded and WHO coordinated “First
International Rapid Response Training for Avian and Pandemic Influenza”
that included more than 100 participants from 14 countries; a
provincial governor said after the announcement that outbreaks
in humans had been ongoing in his district since May and provincial
agricultural officials said that outbreaks had been reported to
officials in . Even in |
cases where national governments
may have international reporting policies and procedures in place
and be proactive in their fulfillment, local and provincial government
officials in countries such as China and Indonesia are known to
be actively suppressing the investigation and reporting of possible
bird flu outbreaks or human cases within their jurisdictions.
Similar processes are evident in multilateral organizations as
well as governments. Recent revelations indicate that the World
Health Organization may be deliberately and routinely suppressing
the reporting of politically-sensitive data on bird flu outbreaks
in humans to the international community. An article published
in the journal NATURE revealed that WHO officials had provided
misleading reports on the presence of genetic mutations found
in the H5N1 virus collected from eight persons from a single family
involved in a human-to-human transmission cluster in Indonesia,
the largest human-to-human transmission H5N1 cluster reported
to date (Butler 2006). WHO failed to report that there been both
primary and secondary human transmission documented within the
cluster, and that had been an unusually high number of mutations
(32) discovered in one of the samples (Butler 2006). The official
WHO report on the gene sequences issued from the human cluster
published on 23 May 2006 announced that the viruses showed no
mutations associated with resistance to the neuraminidase inhibitor
antivirals such as oseltamivir (Tamiflu) and zanamivir (Relenza)
(WHO 2006), but failed to report the discovery that viruses in
the human-to-human cluster had the genetic mutation that provides
resistance to adamantane antivirals such as amantadine and rimantadine
even though this mutation is rarely seen in H5N1 viruses from
Indonesia (Cheung et al 2006).
Conclusions
Pandemic response planning processes based on the assumption
that countries will be either able or willing to rapidly confirm
and subsequently report outbreaks of dangerous diseases to the
international community are unlikely to be successful under current
conditions, and contingency preparedness plans must account for
the fact that disease outbreaks involving H5N1 or other economically-important
disease will not be reported either proactively or voluntarily
by most countries around the world. We must enhance the effectiveness
of global medical surveillance networks for the H5N1 bird flu
virus and other dangerous human-transmissible emerging or re-emerging
disease pathogens, and increase the use of open-source intelligence
gathering and analysis techniques to provide valuable indicators
and reliable warnings of outbreaks of dangerous pathogens whose
reporting may be suppressed by local, national, and/or international
authorities for reasons of policy, economic trade issues, or national
pride.
The sequence and timing of events that have unfolded during H5N1
epizootic have demonstrated repeatedly that potential suspected
outbreaks in poultry or wild birds may not be reported by farmers
or local officials because of economic concerns, and that even
when reported, such outbreaks may not investigated in a timely
fashion by agriculture or public health officials due to reluctance
to reveal the existence of potential outbreaks or a lack of technical
capacity to perform a |
| thorough investigation. Even in those cases
where outbreaks have been investigated and confirmed, the reporting
of laboratory confirmations of H5N1 cases in birds or human by governments
and multilateral organizations may be delayed or suppressed for
policy or economic reasons, or -- in the case of public sector and
private sector scientists and institutions -- for reasons of data
control and publication priority.
Without greater international cooperation and coordination of
H5N1 surveillance and control efforts, we are unlikely to be able
to prevent the further spread and proliferation of this pathogen
throughout the remaining unaffected areas of Eurasia and Africa,
or forestall its introduction and subsequent establishment in
Australasia and the Americas. Animal and human disease surveillance
programs need to integrate and coordinate the monitoring and testing
of wildlife, food animals, farm animals, and household pets. We
must greatly reduce the time required to confirm and report H5N1
bird flu infections in birds and humans, and decrease the potential
mechanisms by which human-transmittable disease pathogens can
be transported through domestic and international, legal and illegal,
commercial trade and transportation networks. We need to increase
public understanding of the level and degree of biosecurity and
public health threats presented by avian influenza viruses and
other human-transmittable animal diseases, and to increase the
capacity of countries worldwide to prevent, detect, diagnose,
and contain disease outbreaks in avian, animal and human populations.
Acknowledgements
The information database upon which this analysis was based was
developed under funding from the Institute for Defense and Homeland
Security, Kansas State University - National Agricultural Biosecurity
Center, United States Department of Agriculture / Animal and Plant
Health Inspection Service, General Dynamics Corporation, and Intellibridge
Corporation.
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