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Appendix B
Surveillance and Response of Select
Zoonotic Disease Outbreaks
WILDLIFE TRADE AND THE HUMAN MONKEYPOX
OUTBREAK IN THE UNITED STATES
Multistate Epidemiological Investigation
The first U.S. outbreak of human monkeypox was reported in May
2003 and initially included cases in Wisconsin, Indiana, and Illinois. By the
end of the outbreak in June 2003, there were reports of cases in Missouri,
Kansas, and Ohio (CDC, 2003a). As of July 31, 2003, there were 72 re-
ported cases, of which 37 were laboratory confirmed (CDC, 2003b). Epi-
demiological and trace-back investigation by local, state, and federal public
health authorities found that patients acquired the disease from prairie dogs
in contact with human monkeypox-infected African rodents (CDC, 2003b).
These prairie dogs were housed together with infected African rodents in
an Illinois wholesale pet store. Approximately 200 prairie dogs were in this
facility and possibly exposed to human monkeypox in the period between
when the Illinois animal distributor purchased the African rodents and the
first reported human case of human monkeypox. A Texan animal distribu-
tor legally imported the infected rodents (762 rodents that included rope
squirrels, tree squirrels, Gambian giant rats, brush-tailed porcupines, dor-
mice, and striped mice) from Accra, Ghana (CDC, 2003a). These rodents
were not screened for disease before or after they entered the United States.
Of this shipment, 23 percent of the imported rodents could not be traced
beyond the port of entry because records were not available. Before labo-
ratory confirmation, trace-forward investigations suspected these rodents
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GLOBAL SURVEILLANCE AND RESPONSE TO zOONOTIC DISEASES
were the source of human monkeypox. This investigation determined that
no other U.S. animals besides prairie dogs were infected with human mon-
keypox (CDC, 2003b). Finally, clinical studies concluded that respiratory
and direct mucocutaneous exposures were important routes of transmis-
sions between infected prairie dogs and humans (Guarner et al., 2004).
CDC and FDA Restrictions of Rodents from Africa
On June 11, 2003, the Centers for Disease Control and Prevention
(CDC) and Food and Drug Administration (FDA) jointly issued an order
pursuant to 42 C.F.R. 70.2 and 21 C.F.R. 120.30, respectively, to restrict
the “transportation or offering for transportation in interstate commerce,
or the sale, offering for sale, or offering for any other type of commercial
or public distribution, including the release into the environment of”
prairie dogs, tree squirrels, rope squirrels, Gambian giant rats, dormice,
brush-tailed porcupines, and striped mice (CDC, 2003a; FDA, 2008). In
addition, pursuant to 42 C.F.R. 71.32(b), CDC implemented an immediate
embargo on the importation of all rodents from Africa. Because the ac-
tions taken by state health authorities were insufficient to prevent the
spread of human monkeypox, CDC and FDA issued an interim final rule
(42 C.F.R. 71.56 and 21 C.F.R. 1240.63 respectively) under section 361
of the Public Health Service (PHS) Act that was intended to prevent future
introduction, establishment, and spread of the human monkeypox virus
in the United States. Based on risk-assessment of the further transmission
of the human monkeypox virus, FDA removed its regulation in 21 C.F.R.
1240.63 in 2008 and concluded that CDC’s interim final rule and routine
state disease surveillance and preventive measures were sufficient to pre-
vent new human and animal cases of human monkeypox. Under section
368(a) of the PHS Act, any person who violates a regulation prescribed
under the Act may be punished by imprisonment for up to 1 year or fined
up to $100,000 per violation if death has not resulted from the violation
or up to $250,000 per violation if death has resulted. Organizations may
be fined up to $200,000 per violation not resulting in death and $500,000
per violation resulting in death (FDA, 2008).
Reemergence of Human Monkeypox in Africa
The virus that causes human monkeypox was first isolated in 1958
from monkeys and recognized as a new virus of the genus Orthopoxvirus
(same genus as the smallpox virus although different epidemiologically and
biologically) (Guarner et al., 2004). Human monkeypox, however, was first
identified in humans in 1970 in the tropical areas of the Democratic Repub-
lic of the Congo (DRC) (Breman, 2000; CDC, 2003a). The first outbreaks
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APPENDIX B
of human monkeypox occurred in the period of 1970–1980 in the DRC,
Côte d’Ivoire, Liberia, Nigeria, and Sierra Leone. Active disease surveillance
was implemented with the assistance of the World Health Organization
(WHO) in 1981–1986 in the DRC, where most of the human cases during
this period occurred. Reporting of human monkeypox decreased, and after
1992 no new cases were reported to WHO. Failure to maintain disease
surveillance of human monkeypox contributed to the reemergence of the
disease in the DRC in 1996. Epidemiological and laboratory investigation
of the DRC outbreak concluded that the disease was mild but highly trans-
missible (Heymann et al., 1998).
UK GOVERNMENT REGULATORY RESPONSE TO CONTROL
BOVINE SPONGIFORM ENCEPHALOPATHY (BSE)1
In 1986, when BSE was identified as a new disease, the Ministry of
Agriculture, Fisheries and Food (MAFF) was the government agency re-
sponsible for overseeing state veterinary services under the State Veterinary
Service for Great Britain, composed of the Veterinary Investigation Ser-
vice (VI Service), the Veterinary Field Service, and the Central Veterinary
Laboratory (CVL). The VI Service implemented surveillance and provided
expert advice for veterinary surgeons in private practice about unknown
animal diseases. Employees of the VI Service reported to the assistant chief
veterinarian and the chief veterinary officer at MAFF.
MAFF and its agencies, prior to the identification of BSE, relied on
a passive surveillance system for the identification of new diseases in
animals. The surveillance of nonnotifiable diseases was based on the ob-
servations of an astute farmer and veterinarian, who would voluntarily
notify one of the many Veterinary Investigation Centers (VICs) of the VI
Service.
December 22, 1984—David Bee, a local private veterinarian, was called to
examine Cow 133, owned by Peter Stent of Pitsham Farm in Sussex. Cow
133 developed a head tremor and a lack of coordination before dying on
February 11, 1985. Bee sought assistance from J. M. Watkin-Jones, a vet-
erinarian at the Winchester VIC, one of the branches of the VI Service.
September 13, 1985—Carol Richardson, the pathologist on duty at the
CVL, received samples of brain, spinal cord, and kidney of Cow 142 and
examined them. Cow 142 was also owned by Stent and was showing ner-
vous clinical signs similar to Cow 133. Richardson shared the sample with
her colleagues at the CVL Pathology Department. Initially, the pathologi-
cal examination suggested that the cause of the disease was not acute, but
chronic bacteremia or endotoxemia.
1 The BSE Inquiry (2000).
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0 GLOBAL SURVEILLANCE AND RESPONSE TO zOONOTIC DISEASES
April 1985—Colin Whitaker, a private veterinarian, was called to Plurenden
Manor Farm in Kent to look at a cow. He sent the cow to the University
of Bristol Veterinary School at Langford, and postmortem examination
showed “progressive nervous signs, hyperesthesia, tremors, mania and
hind leg ataxia.”
November 1986—Whitaker consulted Dr. Carl Johnson, veterinary officer
of the Wye VIC, who referred the brains of the three animals to the CVL
in November and December 1986.
December 11, 1986—The CVL also received brain samples from a cow
that was referred by Langford VIC, in Bristol. In December 1986, after
the identification of BSE as a novel disease by CVL scientists, Dr. Watson,
CVL director, informed William Rees, chief veterinary officer at MAFF,
about BSE. In June 1987, new knowledge regarding the pathology and
epidemiology of the disease led to the notification of this new disease to
other ministers and government officials. After the preponderance of the
evidence at the time regarding the risks posed by this novel disease to hu-
man health, the government implemented a series of regulations aimed at
the animal feed and rendering industry as well as slaughterhouses.
Because it was initially understood that BSE was spread through ani-
mal feed, in June 1988, the Bovine Spongiform Encephalopathy Order
1988 introduced a ban of ruminant feed in addition to the compulsory
notification of BSE. The Order, which came into effect on July 18 and
only applied to Great Britain, required farmers or their veterinarians to
notify the local Divisional Veterinary Officer if they suspected an animal
was affected by BSE. At this point, MAFF would send one of its own
veterinarians to investigate. The ruminant feed ban included the follow-
ing provisions:
(1) No person shall knowingly sell or supply for feeding to animals any
feedstuff in which he knows or has reason to suspect any animal protein
has been incorporated.
(2) No person shall feed to an animal any feedstuff in which he knows or
has reason to suspect that any animal protein has been incorporated.
On August 8, 1988, two further Orders came into effect: The Bovine
Spongiform Encephalopathy (Amendment) Order 1988 and The Bovine
Spongiform Encephalopathy Compensation Order 1988. They introduced
a policy of compulsory slaughter of BSE-infected animals and payment of
compensation to the owner of the slaughtered animal.
On November 13, 1989, the Bovine Offal (Prohibition) Regulations
1989 came into effect in England and Wales. This regulation prohibited
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APPENDIX B
the use of specified bovine offal (SBO) in the preparation of food for hu-
man consumption after findings showed that particular cattle organs were
most likely to carry the infective agent. SBO included the brain, spinal
cord, thymus, spleen, tonsils, and intestines from a bovine animal more
than 6 months of age. One of the unintended consequences of this ban was
that renderers (rendering is the process of converting animal byproducts
into more useful materials, e.g., purifying fatty tissue into lard or tallow)
demanded that mechanically recovered bovine meat (MRM) should not
contain SBO, and thus no longer welcomed cow heads containing the brain.
As a result, a practice rapidly developed at many slaughterhouses of split-
ting the skull and removing the brain. This practice gave rise to problems of
contamination. Later on, review of the SBO ban revealed a concern about
the risk that slaughterhouse practices would result in the contamination
of MRM. MAFF officials assumed that the regulations up to 1989 would
have reduced the scale of infection to a fraction of that at the height of the
epidemic.
However, many more animals born after the ban (BAB) were diag-
nosed with BSE, which showed proof of the limitation and problems in
the implementation of the BSE legislation up to 1989. The first case of
BSE in an animal born after the introduction of the ruminant feed ban
was not confirmed until March 1991. By September 1992, the number of
BABs had risen to 220. By September 1994, the total number of BABs had
reached 12,860. It was concluded that BABs had been fed contaminated
feed. Based on the finding, more aggressive regulatory measures followed
in the period 1994–1996 to prevent the spread of the disease and to protect
human health.
The UK BSE epidemic forced changes in different sectors of the animal
and food production industry. First, regulations of the rendering industry
changed the rendering processes, and, as a result of BSE, meat and bone
meal is no longer used in the United Kingdom in animal feed or as fertilizer.
Second, the introduction of regulations of the animal feed industry affected
the industry but was an essential part of control of the disease. Third, it was
considered essential that slaughterhouses separated SBO from those parts
of the carcass that were going to enter the human food chain. All these in-
terventions underscore that the risk of disease or contamination was in the
processing of animal materials, which put humans at risk at many different
points of this process.
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GLOBAL SURVEILLANCE AND RESPONSE TO zOONOTIC DISEASES
February 23, 2003: CDC
February 27, 2003:
and WHO experts arrive in
Chinese Ministry of Health
Beijing. Chinese authorities
declares the epidemic is
November 16, 2002: First do not authorize the team of
contained. Government
case of SARS is recorded experts to travel to
officials in Beijing order that
in Foshan, Guangdong Guangdong Province and
information about the
Province, China. Chinese limit their access to official
disease spread should not
authorities initially data. The active efforts of
be disclosed, treating this
characterize the first SARS government officials in
information as “top secret.”
cases as an atypical Beijing to suppress
Attempts to suppress
pneumonia and suspect knowledge of the outbreak
information fail when on
that the causative agent is and the spread of the
April 4, the health director
an influenza virus. In disease within China
of China’s Center for
January 2003, Guangdong compromise the
Disease Control apologizes
health authorities release a international response,
to China’s citizens about
report with details of the especially the investigations
the agency’s failure to
outbreak, but official on the magnitude and risk
inform the public about the
confirmation to WHO is of an international spread of
threat of this new disease.
provided on February 14. the disease.
February 21, 2002: The February 26, 2003: A man
first known SARS case is with respiratory symptoms
reported in Hong Kong. A who had stayed at the
medical doctor who had Metropole Hotel in Hong
treated patients in Kong before arriving in
Guangzhou in the Vietnam is admitted to a
Guangdong Province hospital in Hanoi. After an
arrives at the Metropole increase in the reports to
Hotel in Hong Kong where WHO about the spread of
he infects 16 individuals. the atypical pneumonia in
hospital personnel in Hong
Kong and Vietnam, WHO
sends an emergency alert
to Global Outbreak Alert
and Response Network
partners on March 12.
FIGURE B-1 National and international response to the SARS outbreak.
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APPENDIX B
March 15, 2003: WHO
issues Global Travel
Advisory. Before the
identification of the April 3, 2003: WHO expert
causative agent, the virus team finally arrives in
spreads within 6 months to Guangdong Province. The
30 countries and next day, U.S. President
administrative regions. The George W. Bush signs
virus transmission along executive order adding
five major airline routes by SARS to the list of
the symptomatic individuals quarantinable
traveling from Hong Kong to communicable diseases,
Beijing, Hanoi, Singapore, which provides CDC July 5, 2003: WHO
Taiwan, and Toronto with legal authority to announces the global
accelerates the global implement isolation and containment of the SARS
spread of SARS. quarantine measures. outbreak.
March 27, 2003: WHO April 16, 2003: WHO
issues recommendation of laboratory network
exit screening of announces conclusive
passengers at airports. identification of new
coronavirus as the
causative agent for SARS.
The Chinese government
increases transparency
through the release of
number of cases in each
Province, in addition to daily
updates. Moreover, based
on media reports, more
than 120 officials were
dismissed, including the
health minister and Beijing’s
mayor, or penalized for
ineffective response to the
outbreak.
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GLOBAL SURVEILLANCE AND RESPONSE TO zOONOTIC DISEASES
HIGHLY PATHOGENIC AVIAN INFLUENZA H5N1
SURVEILLANCE IN HONG KONG AND VIETNAM
H5N1 Virus Evolution
Highly pathogenic avian influenza (HPAI) H5N1 virus is the causative
agent for millions of bird deaths in Southeast Asia, the Middle East, Eu-
rope, and Africa. The natural reservoir of the influenza type A virus is wild
waterfowl, but the virus can also infect domestic poultry and humans and
cause illness and death, thus the high pathogenicity of the virus (Nguyen et
al., 2005). Virus typing and serological identification tests have indicated
that different strains of type A influenza H5N1 are responsible for illness
and death in humans in Southeast Asia since the Hong Kong outbreak in
1997 (Wan et al., 2008). This outbreak was characterized by a 10 percent
incidence of HPAI H5N1 infection in live-bird market poultry workers
exposed to infected domestic birds housed in close contact with wild wa-
terfowl (Nguyen et al., 2005). After the Hong Kong outbreak, the virus
spread to other countries in the region more likely through the poultry
trade. Although the H5N1 virus has reassorted many times, all these viruses
carry the same H5 hemagglutinin (HA) gene, which has a central role in
antigenic drift. In Vietnam, isolation of the H5N1 virus shows six different
HA clades, thus suggesting that the virus has been introduced at least six
times since the first isolation in poultry in 2001 (Wan et al., 2008).
Response to HPAI H5N1 Outbreak in Hong Kong
In 1997, Hong Kong health authorities quickly instituted strong con-
trol measures in poultry to minimize or stop human exposures (Webster,
2004). These measures included slaughter of 1.6 million chickens present
in wholesale facilities or vendors within Hong Kong; banning importation
of chickens from neighboring areas; instituting serological monitoring of
chickens in Hong Kong; marketing chickens separately from other avian
species; separating chickens and ducks for transport to market; slaughtering
chickens and ducks separately; changing the operation and management
of the live market system such that aquatic birds were no longer housed
and sold in Hong Kong live bird markets, rather they were made available
for sale only as killed, chilled poultry; serologically screening all poultry
imported for sale in Hong Kong for avian influenza virus H5 subtype anti-
body prior to release for sale; and instituting measures to improve hygiene
in the markets. Further interventions were instituted that included estab-
lishing surveillance in live poultry markets and in poultry at the Chinese
border at which each arriving flock was quarantined, tested, and held for
2 days, flocks with one or more sick birds were rejected, and clean flocks
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APPENDIX B
were moved to a central wholesale warehouse and held for 2 or more days.
Culling was carried out on an ongoing basis as necessary; monthly rest days
in live bird markets were instituted where unsold poultry in retail markets
were killed, markets were left empty a whole day, cleaned, and restocked
with fresh poultry the next day; and birds were vaccinated in outbreak
situations. Transmission of the virus and further outbreaks in poultry were
controlled and stopped.
During 1998–2003, isolated outbreaks of HPAI H5N1 in poultry oc-
curred in Southeast Asia; however, it was not until mid-2003, when more
widespread outbreaks in poultry occurred in South Korea. There were
significant delays in international reporting, and weaker response measures
were instituted and the virus began to spread across Southeast Asia. Addi-
tional outbreaks in poultry and human cases of HPAI were next identified
in Vietnam in 2003.
HPAI H5N1 Outbreaks in Humans and Animals in Vietnam
HPAI infection in humans was first officially reported in Vietnam in
January 2004; subsequently the country has endured six waves of epi-
zootics of HPAI H5N1 in poultry (Vu, 2009). In 2003–2004, two waves
of outbreaks in poultry affected many provinces (56 provinces reported
outbreaks during the first wave and 17 provinces during the second wave),
which resulted in the death by infection or culling of more than 44 mil-
lion birds (Sims, 2007; Vu, 2009). During the third wave from December
2004 to April 2005, outbreaks were reported in 36 provinces, with about
2 million birds killed. At this time, the government implemented a pilot
vaccination campaign and was recommending a nationwide vaccination
(Vu, 2009). During the fourth wave from October to December 2005, 21
provinces reported outbreaks in poultry, which resulted in a loss of 4 mil-
lion birds. In 2006, the virus activity was low mainly due to mass vaccina-
tion of poultry in the previous year; however, new reassorted viruses were
still circulating at low levels (Wan et al., 2008). From December 2006 to
November 2007, the reemergence of virus was reported in poultry in more
than 20 provinces and resulted in a loss of 270,000 birds. Recent reports
indicate that a sixth wave of outbreaks occurred from December 2007 to
March 2008 (Vu, 2009). In March 2009, the government reported eight
outbreaks in six more provinces.
Vaccination of Poultry in 2005
In October 6, 2005, the government of Vietnam launched the vaccina-
tion campaign nationwide (Vu, 2009). The goal of vaccination was to re-
duce the number of susceptible poultry, raise the immunological resistance
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GLOBAL SURVEILLANCE AND RESPONSE TO zOONOTIC DISEASES
to virus, and reduce the amount of the virus that immune-infected poultry
can excrete (Sims, 2007). In mid-2005, the government also introduced
a number of control measures such as banning of duck breeding, public
awareness campaigns, and the closure of urban markets in addition to
restricting culling to known infected flocks in order to reduce the risk of
infection to HPAI H5N1 viruses (Van Nam, 2007). The next year, in 2006,
scientists suggested that the lower activity of virus was due to vaccination.
Postvaccination disease surveillance provided evidence that the mass vac-
cination program and other control measures were successful in control-
ling transmission to humans, as there were no reported cases of disease in
humans in 2006. On the other hand, vaccination activities resulted in a shift
to passive disease surveillance of the virus, which assumed the eradication
of the virus in Vietnam and bordering countries. However, the emergence
of the virus in 2007 and later years demonstrates the systematic failure to
detect the new variants circulating in Vietnam, although at lower levels,
previous to the 2007 outbreak. Although vaccination was important in
reducing the virus genetic reservoir, the experience in Vietnam demonstrates
that strengthening disease surveillance in poultry is an essential component
of the strategy to be able to prevent and control the introduction of new
HPAI H5N1 strains into the country (Wan et al., 2008).
Response Measures and Impacts on Human
and Animal Morbidity and Mortality
Although Vietnam is one of the countries most affected by HPAI H5N1,
the response measures have been successful in controling new infections in
poultry and preventing transmission to humans. Additionally, there was a
cost benefit of implementing vaccination in poultry versus mass culling of
poultry. However, the World Organization for Animal Health has recently
emphasized the need for an exit strategy in places where vaccination is be-
ing used as a control measure that have been able to improve veterinary
services and biosecurity measures (OIE, 2009). Some experts believe eradi-
cation of HPAI H5N1 would be difficult to achieve and thus many countries
will continue to use vaccination for many years (Sims, 2007). This means
that a mass vaccination program may be unsustainable, especially due to
the high costs and the limited number of field staff as in the case of Viet-
nam. However, Vietnam has taken steps to review their current vaccination
policies and explore the option of more targeted vaccination of poultry.
It has also recognized the importance of postvaccination disease surveil-
lance, especially in monitoring the effects of vaccination on emergence of
virus variants. As of July 1, 2009, 436 human cases of HPAI H5N1 and
262 deaths have been reported from 15 countries (WHO, 2009a). Despite
further surveillance and response efforts instituted in poultry by human
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APPENDIX B
and health authorities of affected countries, poultry outbreaks and human
cases continue to occur.
WEST NILE VIRUS OUTBREAK IN NEW YORK CITY2
West Nile virus (WNV) first appeared in birds around mid-June of
1999 when veterinarians at Bayside veterinary clinic in the Flushing neigh-
borhood of Queens identified neurological disorders in crows. By mid-
August, dead crows were sent to the state Department of Environmental
Conservation (DEC), which had jurisdiction over wildlife, for necropsy
examinations. Parallel to the bird deaths in Queens, numerous crows and
other birds were dying in and around the Bronx Zoo, prompting veterinar-
ians at the zoo to send dead birds to the DEC for examination. The chief
pathologist at the Bronx Zoo, however, believed that the DEC wildlife
pathologist’s determination of the cause of deaths of bird specimens from
Queens was not correct since it was not based on histopathology, and
therefore decided to initiate her own necropsy on zoo birds, which showed
possible encephalitis. Only days later, a separate epidemiological investiga-
tion of suspected human cases of viral encephalitis was initiated by the New
York City Department of Health (DOH) Bureau of Communicable Disease.
An initial investigation by city public health officials revealed a cluster of
human cases with the same symptoms; subsequently the city DOH noti-
fied the state health department and CDC for additional assistance. After
conversations with CDC and the state health department, city health of-
ficials sent patient specimens to the state virology laboratory for examina-
tion. Field investigations revealed the presence of Culex pipiens mosquito
breeding sites and larvae in many of the patients’ homes and in the Queens
neighborhood, reinforcing the theory of viral encephalitis.
In early September 1999, public health and veterinary authorities con-
tinued to conduct two separate investigations. The human outbreak inves-
tigations involved multiple laboratory facilities (state and federal), public
health officials at the local, state, and federal level, and city government
officials. On the animal side, mainly state wildlife scientists and Bronx Zoo
veterinarians conducted investigations of the deaths in birds. On September
2, 1999, state laboratory tests were positive for a flavivirus; specifically the
test showed a strong serological reaction to St. Louis Encephalitis (SLE)
virus, results that were confirmed the next day by the CDC Division of
Vector-Borne Infectious Disease laboratory in Fort Collins, Colorado. The
same day, city officials announced CDC’s confirmation of an SLE outbreak
in New York City and the decision to initiate mosquito control activities.
At this point of the human outbreak investigation, communications
2 GAO (2000); Fine and Layton (2001); Scott (2002).
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GLOBAL SURVEILLANCE AND RESPONSE TO zOONOTIC DISEASES
between federal, state, and local public health officials were consistent.
However, key public health officials were not aware of the early events in
birds, especially the neurological disorders identified by local veterinarians
and the increased deaths of birds in the Bronx Zoo. City public health of-
ficials first became aware of the bird deaths after news report on the SLE
outbreak resulted in calls to the bureau hotline. On the other hand, after lis-
tening to news reports of an SLE outbreak in Queens, the Bronx Zoo chief
pathologist began to suspect a possible link between the bird deaths and
human cases of SLE and decided to send specimens directly to the National
Veterinary Services Laboratory (NVSL), a U.S. Department of Agriculture
(USDA) reference laboratory located in Ames, Iowa.
After multiple efforts by the Bronx Zoo chief pathologist to send zoo
specimens to the CDC laboratory in Fort Collins, the laboratory scientists
accepted to examine the bird specimens from the Bronx Zoo. Still the pri-
ority of the CDC laboratory in Fort Collins was to not only process thou-
sands of samples from hospitals but also confirm the initial SLE diagnosis
through lengthy viral neutralization tests, which required isolation of the
virus and polymerase chain reaction (PCR). Although some of these tests
reveal questions on the accuracy of the diagnostic tools, the CDC labora-
tory did not reconsider the SLE diagnosis until the NVSL notified them
that they had successfully isolated a flavivirus from one of the Bronx speci-
mens and other specimens received from the state DEC. At the same time,
independent analyses of human specimens by the New York State (NYS)
DOH virology laboratory resulted in a negative PCR reaction for SLE.
In addition, in a meeting between state and city health officials and CDC
the participants raised questions about the accuracy of the results from
serologic tests performed on specimens of suspected and confirmed cases.
The issue of test accuracy was again raised in a meeting of an independent
working group studying encephalitis from unknown origin in which NYS
health officials and CDC participated. By the end of the meeting, it was
agreed that the NYS DOH would share specimens of human brain tissue
with Dr. Ian Lipkin, an academic researcher from University of California
at Irvine attending the meeting. Around the same time, independent efforts
by the Bronx Zoo chief pathologist resulted in the involvement of the U.S.
Army Medical Research Institute of Infectious Diseases (USAMRIID).
Parallel to the independent investigations by Dr. Lipkin and USAMRIID,
a Fort Collins scientist began PCR testing on human specimens after PCR
tests on bird specimens received from NVSL resulted in high reactivity to
West Nile virus. Almost simultaneously to the CDC laboratory’s confirma-
tion of WNV in birds, Dr. Lipkin informed the NYS DOH that the identity
of the flavivirus could be either WNV or Kunjin virus. Finally, on September
27, 1999, CDC announced that the human outbreaks in New York City
were due to West Nile virus.
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APPENDIX B
Although the delay in diagnosis of WNV did not have an effect on the
response to the human outbreak, especially since mosquito control activi-
ties had been implemented, some experts suggest that the failure of public
health and veterinary authorities to recognize the unexpected increase of
neurological disorders and deaths in birds as potential index cases of a
new outbreak in that animal population lead to the establishment of WNV
in the area and ultimately its spread. Moreover, the need for laboratory
facilities able to test for animal diseases and the insistence of the Bronx
Zoo pathologist in the linkage between the deaths in birds and the SLE
outbreak resulted in the convergence of these parallel investigations. The
lack of communication linkages between the animal and human health sec-
tors at the time was an additional barrier. After the WNV outbreak, many
steps have been taken to close this gap and to integrate animal and human
health surveillance in New York City. In December 2001, the New York
City Health Code added to the Communicable Disease Control Section new
animal disease reporting requirements, which established new procedures
for reporting and controling of animal diseases that are transmittable to
humans or any animal disease of public health importance. In addition,
an invitation to join the Health Alert Network (HAN), an e-mail-based
alert system, was extended to veterinarians and other animal or wildlife
specialists who wish to receive veterinary alerts from the New York City
DOH. Furthermore, the NYS DOH has sponsored several meetings, jointly
with the Veterinary Medical Association, on animal disease surveillance as
part of the efforts to enhance relations with the animal health community
(practicing veterinarians, wildlife specialists, zoo veterinarians, agriculture
agencies, etc.).
INFLUENZA A(H1N1) PANDEMIC, 2009
In the United States, seasonal influenza infections result in high mor-
bidity and mortality in humans, resulting in approximately 36,000 excess
deaths annually. For the most part, these deaths occur in older and younger
people having less developed or compromised immune systems. Pandemic
influenza events have occurred every 40–50 years over the past several
hundred years. During the 20th century, pandemic influenza has occurred
in 1918, 1957, and 1968. The 1918 influenza pandemic caused extremely
high rates of morbidity and mortality, especially in healthy adults between
20–40 years of age. Since 2003, continuing human influenza infections from
HPAI H5N1 have caused great concern over the potential of this virus to
result in the next pandemic. With the high mortality rate observed among
infected patients, human health officials have been worried that should this
virus become easily transmissible, a pandemic with this virus would also be
accompanied by severe illness, morbidity, and mortality.
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0 GLOBAL SURVEILLANCE AND RESPONSE TO zOONOTIC DISEASES
Detection and Identification of Risk Factors
In March and April 2009, influenza caused by a novel influenza
A(H1N1) virus was detected in human populations in Mexico and the
United States (Brownstein et al., 2009). Early results from phylogenetic
studies aimed at determining the genetic composition of the virus (Smith
et al., 2009) found that the virus is derived from combinations of swine
viruses that have been circulating over the past 20 years. Because of this, the
virus was quickly referred to as the “swine flu” by human health authorities
and the media, even though to date, there has been only one known occur-
rence of an outbreak caused by this virus in pigs. The specifics of when and
how this virus emerged, in what populations, how long its circulation has
gone undetected, as well as the source of exposure for the outbreak in pigs
remain the focus of ongoing investigations. This outbreak highlights a need
for more strategic and systematic surveillance of influenza in pigs.
Response
As the new virus was detected and began to spread, health officials in
Mexico quickly decided to close schools and take other actions to limit
opportunities for large groups of people to come together where person-
to-person spread could easily occur. Health officials in Mexico and the
United States quickly launched outbreak investigations to learn more about
the virus, routes of and risk factors for transmission, and the potential for
severe morbidity and mortality. In the United States, local health authorities
based decisions for school closures on information that CDC was provid-
ing in daily updates. As increased numbers of cases were detected, it was
determined that this new virus was spread the same way that seasonal
influenza is transmitted, and although morbidity rates among the exposed
were high, mortality was relatively low. Unfortunately, the name used to
refer to the disease as “swine flu” was not based on actual detection of the
virus in pigs or from human cases resulting from contact with sick pigs.
And despite a joint press release from OIE/FAO and WHO, many people
quickly associated wrongly that they could become infected by eating pork.
The negative impact of the inappropriate naming of the virus on the pork
industry was significant and is described below. However, once this impact
became known to human health authorities, they quickly responding by
changing the name of the virus and infection to novel influenza A(H1N1)
2009, which was greatly appreciated by animal health authorities and the
swine industry. The media, however, continued to inappropriately refer
to the virus as the “swine flu,” causing public confusion about the actual
risk factors for exposure and therefore leading policymakers to base their
responses on factors other than evidence. For example, despite the lack of
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APPENDIX B
evidence of any swine infections, Egypt responded to the outbreak by cull-
ing more than 250,000 pigs in the country.
Outcome and Impact
Human infections are being monitored globally. On June 11, 2009,
WHO declared an influenza pandemic caused by this virus. As of July 6,
2009, pandemic A(H1N1) 2009 virus had been officially reported in 94,512
human cases, caused 429 deaths, and had been found in 99 countries, terri-
tories, and areas (WHO, 2009b). Those under the age of 50 years appeared
to be at increased risk of infection. Work has begun to develop a vaccine
that would be available by the 2009–2010 winter season in North America.
By incorrectly naming a virus transmitted between humans as swine flu, this
has resulted in trade bans and reductions in pork consumption, ultimately
causing losses of approximately $28 million per week to the swine indus-
try (Snelson, 2009; TVMDL, 2009). Given the importance of encouraging
disease surveillance, reporting, and response by the livestock industry in an
effective emerging zoonotic disease surveillance system, these losses based
on misinformation are unfortunate and serve to discourage future coopera-
tion in an integrated surveillance and response effort. The accurate naming
of influenza viruses is significant in reporting and response and critical in
effectively conveying information to protect public health.
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