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Bioterrorism and equids
Bioterrorism and Equids Julie A. Pavlin, MD, MPH, ClaraJ. Witt, VMD, MPH, Donald L. Noah, DVM, MPH, Peter J. Timoney, MVB, MS, PhD, FRCVS
A bioterrorism attack can affect the health of many different populations, even those that were not intended as targets. Whether the aim of an attack ts humans, antmals or crops, the result can be mantfested in many species, including equids. Equlds comprise a multibilhon-dollar industry in the United States, and any disease that affects this trade can have a devastating impact on the economy. In addition, equids could potentially serve as sentinels of an attack against humans, or as amphfymg hosts for certain diseases. Knowledge of what diseases have the greatest potential as bioterronst or agroterronst agents, how they may present, and what preventive measures are needed to stop their spread is the first step in preparedness. Surveillance for disease outbreaks in equids should be ongoing, with immediate reporting of any unusual findings to the appropriate veterinary and public health authorities. Key words: BIoterrorism, veterinary public health, equlds. Copyright 2002, Elsevier Science (USA). All rights reserved.
he recent biological attacks in the United States revealed
T vulnerabilities that we did not anticipate. Prior to Novem-
ber, 2001, many scientists and health professionals did not appreciate the ability of dried spores of Bacillus anthracis to permeate envelopes and spread throughout buildings and infect people via both the cutaneous and inhalational routes. The need to protect workers against such a threat had not been previously considered. For most of the US population, the need to prevent and respond to a bioterrorist attack against our agricultural industry and the equine population in particular had also not been realized, much less appreciated. The threat of agroterror]sm or an attack against the nation's agroindustries ]s not theoretical. Eleven documented incidents of biological warfare, terrorism, or crimes perpetrated against animals have occurred in the 20th century, 6 of them involwng eqmds. 1 In the wake of September 11 th and the anthrax letter attacks, the threat of an act of agroterrorism has assumed much greater importance for both the human and veterinary health communities. On 11 September, the US Department of Agriculture's (USDA) Animal and Plant Health Inspection Service (APHIS) issued a statement emphasizing the need to increase Foreign Animal Disease (FAD) surveillance nationwide.2 The American Veterinary Medical Association's president, Dr James H. Brandt, also highlighted the vulnerabdity of the nation's livestock populations to the introduction of foreign diseases via an
From the Department of Defense Global Emerging Infections System, Walter Reed Army Insbtute of Research, Silver Spnng, MD. Address reprint requests to LTC Julie Pavlln, Division of Preventive Medtcine, Walter ReedArmy Institute of Research, 503 Robert Grant Ave, Silver Spring, MD 20910-7100. Copyright 2002, Elsevier Science (USA). All rights reserved. 1534-7516/02/0102-0000535.00/0 dol:l 0.1053/ctep.2002.34239
act of agroterrorism in a letter to Tom Ridge, Secretary of Homeland Defense. 3 Since its initial discovery in North America in 1999, West Nile virus provides an important example of the abihty of a newly introduced pathogen to spread quickly in the United States. 4 Medical professionals caring for any species need to be increasingly vigilant in helping to prevent, detect, or, if it occurs, treat the victims of a bioterrorist attack. The value of the livestock and poultry industries in the United States is estimated at $50-200 bilhon, with over $50 billion in annual exports. 35 Agriculture is also the largest sector of the US economy, representing 13.3% of the Gross National Product (GNP). 6 The nation's livestock population is also highly susceptible to a range of important FADs. A highly contagious and virulent infectious disease such as foot-and-mouth could wreak economic havoc with losses estimated to exceed $30 billion. 5 In addressing the potential impact that certain exotic diseases could have on the equine population in the United States, consideration should be given to the current significance of the horse industry to the national economy. This is frequently grossly underestimated and seldom fully appreciated. The most recent national study undertaken was for the tax year 1994 and examined the diversity of the industry, with specific regard to the activities that contribute directly to the production of horses or that provide amusement and recreation services involving horses, r Based on an estimated population of 6.9 million equids in the United States and approximately 7.1 million human participants, the goods and services produced by the horse industry were valued at $25.3 billion. It contributed as much as $112.1 billion in gross domestic product and provided an estimated 1,404,400 full-time equivalent jobs. The annual revenue from the sale of horses, ponies, and other equids in the United States has continued to increase, especially in recent years, and is currently close to $2 billion. Before the terrorist attacks on the United States, USDAAPHIS developed a National Emerging Response Program to a Highly Contagious Animal Disease for the United States in partnership with the American Vetermary Me&cal Association, the US Animal Health Association (USAHA) and the National Institute for Animal Agriculture (NIAA). The goal of the program was to assist in education, surveillance, prevention, and response to an agroterrorist attack. 8 However, a survey carried out m 2000 by the Minnesota Department of Health to determine veterinary surveillance capacity for zoonotic bioterrorist agents revealed that some high-priority organisms such as plague and tularemia are not reportable diseases in all states, that 39% of state animal health officials had not been involved in bioterrorist or agroterrorist planning and coordination, and that few efforts to educate veterinarians on bioterrorist Issues had been instituted. 9 The first line of defense agamst bioterrorism is a force of educated professionals who can, in the event of
Clinical Techniques m Equine Practice, Vol 1, No 2 (June), 2002: pp 109-115
109
an attack, recognize the signs of a disease and assist with surveillance and response efforts. This article outlines the classification of agents of potential btoterrorist or agroterrorist importance, describes the most significant threats to the equine population, discusses the potential impact on the equine industry and the national economy, and provides an overview of appropriate surveillance measures.
Category
Agent
A
Agents of Bioterrorist or Agroterrorist Potential
B
Vanola major (smallpox) Bacillus anthracis (anthrax)* Yersmia pestls (plague) Clostridlum botulinum toxin (botuhsm)* Franclsella tularensis (tularemia)* Filovtruses (eg, Ebola and Marburg) Arenavtruses (eg, Lassa and Junto) Coxlella burnetti (Q fever) Brucella species (brucellosis)* Burkholderia mallei (glanders)* Alphaviruses (eg, Venezuelan, eastern, and western encephalitis)* Rtcm toxin from Ricinus communis (castor bean)* Clostndium perfnngens toxin* Food and water-borne pathogens (eg Salmonella species,* Shigella dysentenae, Escherichla coli O157:H7, Vibrio cholerae, and Cryptospondlum parvum) Nipah virus* Hantawruses Tmkborne hemorrhagic fever wruses Ttckborne encephahtls virus* Yellow fever Multidrug-reststant tuberculosis
Biological terrorism is the use of a microorganism, toxin, or bioregulator derived from a living organism to cause death or disease in people, animals, or plants. More recently, the term agroterrorism has been applied to situations involving animals or plants. Compared with various human pathogens that may require special manipulations before they can be used effectively as biological weapons, animal pathogens, including some of equine importance, could be employed without undergoing any prior treatment. Many of the pathogens on the list of potential agroterrorist agents may be responsible for natural outbreaks of disease. It is important, therefore, to differentiate between a natural outbreak of a disease and a disease occurrence resulting from the deliberate introduction of a particular agent or toxin, even though the strategies for treatment and prevention of spread may not differ in either situation. Animals could be the targets of a biological attack, or they could serve as sentinels of a bioterrorist attack directed against humans. After the accidental release of Bacillus anthrac~s spores in a military facility in Sverdlovsk, USSR, in 1979, human cases of disease were reported 4 km downwind of the facility, whereas deaths in sheep and 1 cow due to anthrax were recorded 50 km downwind. 1° Regardless of the intended target° a disease agent may cause significant morbidity and mortality in a susceptible animal population, and, in the case of certain diseases such as Venezuelan equine encephalomyelitis (VEE), amphfication of the disease through animals poses an increased threat to humans. During the Cold War, biological weaponry programs in many countries were focused on agents that had high toxicity or pathogenicity, were easy to produce in bulk, and were stable in the environment or under conventional storage conditions. Irrespective of what approach was taken, most countries developed a similar prioritized list of agents. Of these, B. anthracis, Brucella suis, Coxiella burnetii, the equine encephalomyelitis viruses, and various other arboviruses can cause disease in equids. 11 In addition, toxins such as botulinum toxin and ricin can also cause morbidity and mortality in equids. In 2000 the Centers for Disease Control and Prevention (CDC) issued a plan for preparedness and response to biological and chemical terrorism. ~2 To conserve resources, they recommended targeting preparation activities against certain highly significant biological agents Some biological agents are deemed more critical than others based on how high a risk they pose to nauonal security. The criteria used for evaluation include: 1) how easily the agent can be disseminated or transmitted person-to-person; 2) the potential of an agent to cause high mortality and have a major public health impact; 3) the ability of the agent to cause public panic and social disruption; and 4) whether the agent would require special action for public health preparedness.S"- In the case of an agroterrorist attack that affects animals primarily, or as a secondary consequence of airborne or other means of widespread dissemination, we be1 10
TABLE 1. CDC List of Critical Biological Agents
C
NOTE List from Centers for Dtsease Control and Prevention (CDC). 12 *Disease agents that can cause dtsease in equtds.
lieve that an additional criterion, economic impact, should also be considered when prioritizing preparative activities to deal with such an event. The CDC priorttizes biological agents into 3 categories--A, B, and C--with A posing the greatest threat. The biological agents considered critical by the CDC are listed in Table 1. Smallpox and plague are among the diseases posing the highest risk threats to humans, neither of which are pathogenic for equids. However, other infectious agents such as Hendra virus, vesicular stomatitis virus, and African horsesickness virus are threats to equine health. Using the same criteria as the CDC but including the economic impact of a disease, we have compiled a prioritized threat list for equids (Tables 2, 3, and 4). Clearly, some of these agents are zoonotic and if introduced into the United States could spread to human populations. Other agents, such as dengue virus, Congo-Crimean hemorrhagic fever virus and Shigella spp that do not cause disease in equids should still be of concern because seroconversion or isolation of these disease agents in equtds has been documented. 19
Impact of Bioinvasions on the Horse Industry in light of the considerable economic importance of the US horse industry, it is not difficult to appreciate the tremendous financial impact certain exotic diseases could have were they to be introduced into the country's highly susceptible equine population. How significant an impact a particular disease would have depends not only on the particular infectious agent and its primary route(s) of transmission, but also on the activity category of the horse industry that is principally involved. In the most recent economic impact study of the US horse industry, horses and participants in the industry were categorized into 4 groups by activity--racing, showing, recreation, and other (farm and ranch work, police work, rodeo, polo, and so on). Contributions of each of these categories to the Gross Domestic Product total of $112.1 billion in 1994 were 29% each for racing and showing, 27% for recreation, and the other equine activities accounting for the remaining 15%7 PAVLIN ET AL
TABLE 2. Viral Agents With Potential Agroterrorist Significance for Equids
Agent; Zoonot~c Status
Mode of Exposure*
African horse s~ckness¶ (13-15)
IVn (13,16) IHa p~
D~rect Transmission Expected Case Economic Potential m a Fatality Rate m Likely Agent Occurs Impact on Agroterronsm Clinical Equ~ds From Agroterronst Naturally in Equine Event; H, Between Presentation Agroterronst Potential1the US? Industry:l: Horses; M, to Man m Equ~ds§ Event
Control Measuresll
Unlisted
No#
HNh
H, no; M, no
RL (acute), CV (chronic)
Eastern equine IVan (16), IHa encephalomyeht~s wrus** (16-18) Japanese IVn (16) encephaht~s wrus¶,** (13,19) Venezuelan equine IVan (16), IHan encephalomyeht~s v~rus¶,** (13,17,18)
B, E
Yes,l-i late summer to fall No# (13)
Moderate
H, no; M, no
FE, NE
H~gh, VC, V, I, E, especially for DC pulmonary form H~gh VC, V
Low
H, no; M, no
UA, NE
Low
V
H~gh
H, yes:l:$; M, yes$$
FE, NE
H~gh
PP, VC, V, I
Western equine encephalomyelitis wrus** (16,17)
IVan (16); IHa (17)
B, E
Moderate
H, no; M, no
FE, NE
Moderate to h~gh
VC, V
West Nile fever wrus** (20-23) Hendra wrus¶,** (24-26) Influenza A virus¶,** (16) Rotavlruses** (27) T~ckborne encephaht~s wrus, Iouping ill¶,** (16,18) Vesicular stomatlt~s** (13 14,29,30)
IVa n (16)
Unhsted
Yes, southern and tropical US; rainy season Yes, western and central US, summer to fall Yes§§
H~gh
H, no; M, no
UA, NE
VC, V
IHan IIII IG a ~ II[I IHa,7
C
No#
H~gh
H, yes¶¶; M, yesllll
FE, RL, NE
Moderate to h~gh High
D, E
Yes, sporadic Moderate
H, yes; M, yes
Yes No#
Low Moderate
H, yes; M, yes H, no; M, no (18)
FE, RU, RL, DE DI FE, NE, UA (28)
Yes, especially V, I in foals Low S, V, I Possibly high PP, VC (18,28)
Yes
Moderate
H. yes##; M, yes##
FE, VE
Low
Unhsted B, D, E
IGan D IV~ (28), SC,~ C, D IH,~ ~ P~ (w~th ~nfect~ve blood) IVn (13), Unlisted phlebotomine fly (18), IHa*, SCa?
S, E?, I
VC, V?, I
NOTE. C~tat~onsto references are in parentheses. %, agroterrorism; n, natural; IG, ingestion, pnmarily due to food and water contamination; IH, inhalation of aerosohzed agent; IV, insect vector (T, tick; M, mosquito; F, fly); P, parenteral, through rejection, implantation etc; SC, skin contact, including mucus membrane contact, usually thought to require broken skin. 1-CDC classification as per (12): A, top pnonty agent; B, second level pnority agent; C, tNrd level priority agent, D, known to have been weaponized or under development as a btoterronsm weapon in the past (6); E, c~ted as potential biological terronsm agents (12). SPresumed impact based on 5 cntena (assessment of combination of transmission potential, seventy of disease, public fear, need for special measures, and economic and trade disruption). §AB, abortion; AD, lymphadenopathy (w~th or without ulceration); AN, anorexia; FB, fistulous bursitis; FE, fever; CV, cardiovascular (hypotension, shock, heart failure, cardiac arrest, etc), DE, depression; DI, diarrhea; DB, debilitation; GI, gastrointestinal including cohc; HE, hemorrhage; IM, ~mmunosuppressJon, NE, neurologJc; NU, nodular-ulcerative (abscesses, cutaneous, respiratory etc); NT, necrosis topical; RL, lower respiratory; RU, upper respiratory; SE, septicemia; SP, symmetncal descending flaccid paralys~s; UA, unapparent or asymptomatlc; VE, vesicles. IIAssumptlon of transmission potential: A, antlm~croblals; AT, antitoxin; DC, stnngent decontamination of stable/environment; E, euthanasia/ ehminatlon of infected animal; i, ~solatlon/quarantine; PP, use of personal protectwe precauttons such as gloves, gowns, mucus membrane protection; S, basic sanitation; V, vaccnat~on; VC, vector control; W, clean water supply (water borne diseases). ¶Foreign animal disease (14). #Not seen in the US unless imported. **Disease considered zoonotlc (14). 1-1-in eastern and gulf states; less common than western equine encephalitis or St Louis encephahtis, but more serious in humans (16). $:l:Mechanlcal transmission via biting insects possible (16); direct via aerosol possible (13). §§Recent introduction into the US presumed to be naturally occurring. IIIISuspected but not definitive, role of flying fox spp (25). ¶¶D~rect and very close contact w~th respiratory secretions of infected animals (humans?) believed to be required (26). ##Exposure to vesicular fluids.
O[ all the exotm &seases that could threaten the health and economic well-being of the US horse industry, African horsesmkness and VEE, both vector-borne diseases, have the potential to cause the most serious and devastating epidemics of disease among all categories of eqmds, irrespecuve of use or activity. Furthermore, both diseases would drastically impact the ability of the US to export equids or equine semen throughout the world. An example of how sigmficant this export trade has become, especially in the past 5 to 10 years, can be gauged from the fact that approximately one third of the total sum realized at the world-renowned Keeneland Sales m Kentucky for each of the past 2 years represented overseas purchases, most of which were exported. 43 An inability to maintain this BIOTERRORISM AND EQUIDS
export trade would have major economic repercussions for the horse industry wlth losses in revenue running into several hundreds of millions of dollars per year. The introduction of a highly contagious respiratory-borne pathogen such as a virulent variant of equine influenza virus could have a huge impact on the US racing and show industries. Historically, equine influenza has been responsible for major epidemics wherever the virus has been introduced into previously unexposed and lmmunologically naive populations of equids. The epidemms in South Africa and Hong Kong in 1986 and 1992, respectively, closed down racing m each country for a period of up to 1 to 4 months and resulted m considerable finanmal losses totahng many milhons of dollars. 4~ A similar 111
TABLE 3. Bacterial and Protozoal Agents With Potential Agroterrorist Significance for Equids
Dkely Agroterrenst Potentiali-
Agent Occurs Naturally m the US?
Economic Impact on Equine Industry:l:
Direct Transmission Potential in a Agroterrorism Event; H, Between Horses; M, to Man
Clinical Presentation in Equtds§
Expected Case Fatahty Rate m Equlds From a Agroterronsm Event
H, yes**; M, yes**
rE, RL, NU, GI, HE
Htgh without treatment
A, DC, V?
Moderate
H, yes; M, yes
FB, AB
Unknown, probably low to moderate
A, S, I?
No$:i:
High
H, yes; M, yes
DB, NU
A?, E? I?, DC, PP
SC,~ n D IH,. n IG ~ ~
No:I:~
High
H, yes; M, yes
rE, SE, DB, NU
IG," ~ IH ~
B, D, E
Yes
High especially if resistant
H, yes; M, yes
DI, GI, AB
Moderate to Ngh, chronic carners possible Moderate to high, chronic carriers possible Moderate to high (speciesdependent)
IVn (16), IH, ~
A, D
Yes, In western US
High for H, yes**; M, yes** pneumontc form
rE, AN, DE, RU, DI, AD
Possibly low
B
Yes
Moderate
UA, DI
Low
Agent; Zoonottc Status
Mode of Exposure*
Anthrax (Bacillus
IG, ~n IH, ~ ~ SC ~ IG ~ IH, a ~ SC ~ ~
A, D, E
Yes#
High
B E
Yes
IG,~,~IH~
B, D, E
anthracls) (13,17,31,32) Brucellos~sl]
(Brucella, primarily B
Control MeasuresLI
abortus) t t (16,33) Glanders¶,$$
(Burkholdena malleO (13,17,34) Mellotdosls¶,$:l:
(Burkholdena pseudomallel) (13,16,17) Salmonellosts¶ (Salmonella spp) (13,35,36)
A?, Eg, I?, DC, PP A, I, DC, PP
(16) Tularemia¶
(Franctsella tularensls) (13,37) Cryptospondtosls¶
(Cryptospond/um parvum)
SC, ~ ~ IG~ n IG~ ~
H, yes; M, yes
A, VC, S, PP (for pneumontc) I? A (under investigation), W, S
(38,39,40) *,l-,:]:,§dISymbols and notes as in Table 2. 1]Disease considered zoonottc (14). #Areas of the US w~th neutral or alkaline, calcareous soils can be endemm. **Possible if contact with blood or contaminated animals or carcasses. t~rBrucella spp commonly associated with horses are B abortus and B suls. Brucella spp assoctated wtth b~oterronsm potential are B mefitensis and B suis (17,33) :[:$Forelgn animal disease (14). NOTE. Citations to references are in parentheses.
scenario would likely occur m the United States, given the introduction of a strain of influenza virus against which the country's equine population had not been prevmusly protected. Contagious equine metntis is an example of a contagious, venereally transmissible disease of equids that is currently exotic to the equine population m the Umted States. Were it to be
introduced through an act of agroterronsm, contagious equine metritis could readily spread among mares and stallions and cause major &sruption in the principal centers of horse breeding in the country. It would lead to suspension of breeding operations, restricuon of ammal movement, and considerable financial losses for the horse industry. The inadvertent mtro-
TABLE 4. Toxins With Potential Agroterrorist Significance for Equids
Agent; Zoonotic Status
Mode of Exposure*
Botulism toxin (from
IG, an SC~ IH a
Clostridium botuhnum) (13,17,41 ) Epsilon toxin (from
Economic Impact on Equine Industry:i:
Direct Transmission Potential in a Agroterronsm Event, H, Between Horses, M, to Man
Chn~cal Presentation in Equlds§
H, no; M, no
SP
Likely Agroterronst Potential1
Agent Occurs Naturally in the US
A, D, E
Yes, serotypes B and C most common
Moderate
n
Ricinus communls,
B "~, E?, D
IG, an IH ~
B, D, E
Yes
Moderate
H, no; M, no
GI, RU
D, E
Yes
Moderate
H, no; M, no
NT, IM, NE, CV
pa
castor bean) (13,17)
Trichothecene mycotoxln
IG, "n IH, a pa
Control Measures}l
High in u nvacctnated animals
AT (42)
IG, low; IH, high; P, high
PP
Highly toxic I n horses
IG?, P?
Clostndlum perfnngen ) Rtctn (from
Expected Case Fatality Rate ~n Equlds From a Agroterrorism Event
(-1-2, "yellow ram") (17) NOTE. Citations to references are m parentheses * 1-,$,§,llSymbols and notes as in Table 2.
112
PAVLIN ET AL
duction of contagious equine metritis into the thoroughbred breeding industry in Kentucky m 1978 resulted in an estimated direct loss of $4 million at the time. 44 If the disease were to be reintroduced, either accidentally or through an act of agroterronsm, the economic consequences of such an incursion would be considerably greater in today's world of elevated horse values and higher operational costs and would probably exceed $100 million Apart from the direct economic losses that would ensue from the clinical consequences of certain exotic diseases affecting the US horse population, there would be additional financial losses from denied or restricted export markets. If equine diseases currently exotic to this country were introduced through an act of agroterronsm, it would result in major restrictions on trade in horses and equine semen. Aside from the previously cited examples of African horsesmkness, VEE, or contagious equine metritis, other diseases such as vesmular stomatitis, because of its clinical similarity to foot-and-mouth disease (FMD), would adversely affect the industry's ability to trade internationally until the disease had been effectively controlled. In terms of financial significance, if vesicular stomatitis had occurred in Kentucky in 2001, it would have resulted in a &month ban on the export of horses to countries in the European Union and would have led to an estimated loss of over $125 million. 44 There is a general appreciation of the economic losses that would be directly attributable to the deliberate introduction of a specific equine disease such as African horsesickness or VEE. What is not often recognized, however, is that the US horse industry could also suffer very considerable financial damage if another hvestock species besides equids were the target of the exouc pathogen. This was dramatically illustrated by the devastating impact that the large-scale epidemic of FMD in the United Kingdom had on that country's equine industry. 45 Shortly after the disease was confirmed in February, 2001, essentially all horse racing, showing, and recreational activity was banned for several weeks. Racing and certain other equestrian activities later resumed under very stringent conditions involving controlling movements and the observance of strict disinfection measures. However, eventing, hunting, recreational riding, endurance, and point-to-pointing were suspended for many months while the epidemic continued. Large areas of the countryside were closed to horses. The financial impact of these control measures was felt across the industry. Losses were estimated at over $141 million per month from March through May, 2001. There is little doubt that if FMD were deliberately Introduced into the United States, the direct, indirect, and induced effects of the disease on the horse industry would far exceed those experienced during the 2001 epidemic in the United Kingdom. The impact would be felt at all levels of the industry and could result in significant restrictions on international trade in horses and semen.
Bioterrorism Surveillance and Reporting Commensurate with an enhanced awareness and perception of the risk of bioterrorism or agroterrorism, recognition of the need for improved &sease surveillance has also increased. It is worth considering the potential role of equids in any surveillance program for bioterrorism, regardless of the target species, and the factors that can help to differentiate between natural and intentional disease outbreaks. BIOTERRORISM AND EQUIDS
Outbreaks of certain diseases among equine populations have served as sentinel events for the threat of those diseases for humans. Notable examples include various arthropod-borne encephaliudes such as Japanese encephalitis and VEE. In the case of Japanese encephalitis, because humans and equids are both final hosts, horses infected with the virus do not provide a source of infection for humans. However, in temperate Asia, cases among equids typically precede those in people by at least several weeks. 46 Horses also serve as sentinels for human mfeclions in VEE, but for different reasons. In contrast to the other equine encephalomyelitides, equids infected with VEE virus (subtypes lAB or 1C) develop high viremias and serve as very efficient amplifying hosts of the virus. In consequence, they play an extremely important role in propagating an epidemic of the disease in humans. ~6 Recognition of cases of VEE among equine populations is epidemiologically crincal to identifymg the frequency and geographic distribution of infection with this virus, is Equids are of limited potential as sentinel animals with respect to the &seases most likely to be employed by bioterrorists targeting human populations. Although horses are susceptible to a number of these disease agents, such as B anthracls, Burkholderia malle~, Brucella abortus, Coxiella burnetii, and Burkholderia pseudomallei, the low infection rates and similar incubation periods in horses relative to those in humans, make equids unlikely candidates as sentinels. The first recognitmn of West Nile virus in the United States in 1999 is a case in point. Although certain species of birds, ie, members of the corvid family, were identified as potenually valuable sentinels of the risk of exposure of humans, the initial cases among horses on Long Island, New York, occurred either simultaneous with or after reported human cases. 47 Although the equine cases did not qualify as sentinel events, they do serve to illustrate that the manifestation of a newly introduced disease into a susceptible population may be recognized more easily when animal and human health care practitioners communicate on a frequent basis. Once a disease outbreak ~s recognized, an initial question that should be addressed is whether its origins were natural or intentional. Although the point past which epldemiologic proof becomes legal proof is debatable, 4s a number of guidelines have been put forward that can help differentiate between natural and intentional disease events. 49 50 Among those relevant for animal populations are number of cases, temporal patterns of &sease onset (epidemic curve characteristics), clinical presentation, strain or varmnt of etiologic agent, economic impact, geographic location, morbidity and mortality rate, antimicrobial resistance patterns, seasonal distribution, route of exposure, weather and climate considerations, and concurrence with belligerent activities of potential adversaries. Regardless of the causation of the event, rapid reporting must be accomplished for a response to be effective. Whether the veterinarian, owner, or farm manager initially recognizes the disease, prompt notification must be made to the appropriate authorities. Ideally, the veterinary practitioner should notify the state veterinarian and area federal veterinarian-m-charge. Alternatively, an outbreak of an exotic or new disease may be discovered when clinical necropsy specimens are submitted to a veterinary diagnostic laboratory. Evidence or suspicion that the disease is zoonotic should also involve notification of local and state health departments. Upon notification, epidemiologists and diagnosticians may be deployed to assist local investigators in determining the cause of the epidemic and propose an appropriate course of action to bnng it under control. 1 13
Reporting a potential outbreak of a foreign ammal disease should be camed out with a minimum of delay and should include as much information as possible of the circumstances and nature of the occurrence. The responsibility of information generation and reporting should be a shared responslbihty among the local veterinary practitioner, the state veterinarian, the federal veterinarian-in-charge, and the responding foreign animal disease diagnostician. Where indicated, additional reporting to other state and federal agriculture and health officials will be the responsibility of the state department of agriculture. Informatmn provided should include:
3.
4.
5. 6.
7.
• Complete names and addresses of all farms with affected animals. This should include longitude and latitude informatton as well as the type of operation (eg, breeding, racing, boarding). • The same information for potentially exposed ammals on other farms with contiguous fencing that allows face-to-face contact. • Total numbers of animals, including all species, on these farms. Of that total, how many are affected? -What was the date of onset of the first case? Since that tune, how many others have been affected and where were they located or housed in relation to the index case(s)? • Have any affected animals died? If so, what was the disposition of the carcass? Necropsy summary should include descriptions of the body, skin, head area, respiratory system, cardiovascular system, digestive tract/abdominal cavity, urogenital tract, musculoskeletal system, nervous system, and lymph nodes. • Have laboratory samples been taken and submitted? If so, what samples, how many, and where and when were they sent? • Animal movement history. Were affected animals moved anywhere in the few months preceding this event? If so, where and when? Were other animals on the premises moved during the same period? If so, where and when? • Have there been any reports of associated human Illness among farm owners or staff? • Complete physical examination results of affected animals. This should include descriptions of the body (including temperature, behavior, gait, condition, and general appearance), skin, head area, respiratory tract, cardiovascular system, digestive tract and abdomen, urogenital system, musculoskeletal system, nervous system, and lymph nodes. • Finally, an initial list of differential climcal diagnoses should be included. Only when agricultural commodities such as horses, other livestock species, and even crops are included in national survetllance networks, will the United States be able to recognize and respond to natural and intentional disease outbreaks in a timely fashion. This will require improved veterinarian-physician communication and enhanced ammal disease surveillance and reporting programs. 48 5~
References 1. W~lson TM, Gregg DA, K~ng DJ, et al: Agroterronsm, biological cnmes, and blowarfare targeting animal agriculture. The chnlcal, pathologic, diagnostic, and epidemlologic features of some important antmal diseases. Clin Lab Med 21:549-591, 2001 2. USDA/APHIS: Foreign animal d~sease surveillance increased. Sep1 14
8. 9.
10. 11.
12.
13. 14. 15.
16.
17. 18. 19. 20.
21.
22.
23. 24.
25.
26.
27.
28.
29.
30.
tember 11, 2001. Accessed Jan 11, 2002. URL: http://www. avma.org/sc~enact/fad_survetllance.asp JAVMA News. Message to new Homeland Defense Office: Don't forget US agriculture Nov 15, 2001. Accessed January 11, 2002. URL: http://www,avma.org/onlnews/javma/nov01/sl11501 a.asp United States General Accounting Office" West Nile virus outbreak: Lessons for public health preparedness. Washington, DC, United States General Accounting Office, September 2000, Report No. GAO/HEHS-00-180 Williams JL, Sheesley D: Response to blo-terronsm directed against animals. Ann N Y Acad Scl 916:117-120 2000 Logan-Henfrey L: Mitigation of btoterrorlst threats in the 21 th century. Ann N Y Acad Sci 916:121-133 2000 Anonymous: The economic impact of the horse industry in the United States. National Summary, vol 1. Washington, DC, American Horse Council Foundation, 1996 Adams JB" The role of national animal health emergency planning Ann N Y Acad Scl 894 73-75, 1999 Fitzpatrick AM, Bender JB" Survey of chef livestock officials regarding b~oterrorism preparedness m the United States J Am Vet Med Assoc 217:1315-1317, 2000 Meselson M, Gulllemm J, Hugh-Jones M, et al: The Sverdiovsk anthrax outbreak of 1979. Science 266 1202-1208, 1994 Ashford DA, Gomez TM, Noah DL, et al: Btolog~cal terrorism and veterinary medicine in the United States. J Am Vet Med Assoc 217:664-667, 2000 Centers for Disease Control and Prevention: B~olog~caland chemical terrorism: Strategic plan for preparedness and response. Recommendations of the CDC Strategic Planning Workgroup. MMWR Morb Mortal Wkly Rep 49:1-14, 2000 Merck Veterinary Manual (ed 5). Rahway, NJ Merck, 1979 Catcott EJ, Smlthcors JF (eds): Equine Medtclne and Surgery (ed 2). American Vetennary Publications, Wheaton, IL, 1972 Committee on Foreign Animal D~seases of the Untted States Animal Health Association: African Horse Sickness. Part IV. Foreign Animal Diseases. Accessed Jan 20, 2002. URL: http://www.vet uga.edu/ vpp.gray_book/FAD/afs htm Acha PN, Szyfres B: Zoonoses and Communicable Diseases Common to Man and Animals (ed 2). Washington, DC, Pan American Health Organization, 1989 Casper J, Franz D, Garland T, et al: Bioterrorlsm Agents: Impllcahons for Animals. Baltimore, MD, Baltimore City Health Department, 2001 Amencan Public Health Association: Control of Communicable Diseases Manual. Baltimore, MD, United Book Press 2000 Ellis PM, Daniels PW, Banks DK: Japanese encephahtls. Vet Clln North Am Equine Pract 16:565-578, 2000 Komar N, Panella NA, Boyce E: Exposure of domestic mammals to West Nile Virus dunng an outbreak of human encephalitis, New York City, 1999. Emerg Infect Dis 7:736-738, 2001 Gubler DJ, Campbell GL, Nascl R, et al: West Nile Virus in the United States: Guidelines for detection, prevention, and control. Wral Immunol 13:469-475, 2000 Martin AA, Gubler DJ: West Nile encephalitis: An emerging disease in the United States. Clln Infect Dis 33:1713-1719, 2001 Ostlund EN, Crom RL, Pedersen DD, et al: Equine West Nile encephalitis, United States. Emerg infect Dis 7:748-750, 2001 Equine Morb~lhvlrus Pneumonia Part IV. Foreign Animal D~seases. Accessed Jan 14, 2002. URL: http://www.vet.uga.edu/vpp/gray_book/FAD/emp.htm Mackenzie SJ, Chua KB, Daniels PW, et al' Emerging wral diseases of Southeast Asta and the Western Pacific. Emerg Infect Dis 7:497504, 2001 (suppl 3) Barclay A J, Paton DJ. Hendra (equine morbllhvlrus). Vet J 160:165166, 2000 Kojima K, Tan~guchl K, Kobayashi N: Species-specific and mterspecles relatedness of NSP1 sequences ~n human, porcine, bovine, feline, and equine rotavlrus strains. Arch Virol 141"1-12, 1996 Timoney PJ, Donnelly W J, Clements LO, et al: Encephalitis caused by Iouplng Ill wrus m a group of horses in Ireland. Equine Vet J 8:113-117, 1976 McCluskey BJ, Hurd HS, Mumbord EL: Review of the 1997 outbreak of vesicular stomatitls in the western United States. J Am Vet Med Assoc 215:1259-1262, 1999 McCluskey BJ, Mumford EL: Vesicular stomat[tls and other vesicular, PAVLIN ET AL
31.
32.
33.
34. 35.
36. 37.
38. 39.
49.
erosive, and ulcerative d~seases of horses. Vet Chn North Am Equine Pract 16:457-469, 2000 Acha PN, Szyfres B: Zoonoses and Communicable Diseases Common to Man and Animals, vol 1 (ed 3). Washington, DC, Pan American Health Organization, 2001 Hunter L, Corbett W, Gnndem C: Anthrax. J Am Vet Med Assoc 1995. Accessed Jan 19, 2002. URL www.avma.org/press/terronstattacWzu_anthrax.asp Centers for Disease Control and Prevention: Suspected brucellosis case prompts investigation of possible bloterronsm-related act i v i t y - N e w Hampshire and Massachusetts, 1999. MMWR Morb Mortal Wkly Rep 49:509-512, 2000 Glanders, Part IV, Foreign Animal Diseases Accessed Jan 19, 2002. URL: http://www/vet.uga.edu/vpp/gray_book/FAD/gla.htm Schott HC, Ewart SL, Walker RD, et al An outbreak of salmonellosls among horses at a veterinary teaching hospital. J Am Vet Med Assoc 218:1152-1159, 2001 Murray MJ: SalmonellosLs in horses. J Am Vet Med Assoc 209:558560, 1996 Rohrbach BW: Tularemia J Am Vet Med Assoc 1995. Accessed Jan 19, 2002. URL: www.avma.org/press/terronst_attacWzutularemla. asp Mosler DA, Oberst RD: Cryptospondlos~s. A global challenge. Ann N Y Acad Scl 916:102-111, 2000 Atwlll ER, McDougald NK, Perea L: Cross-sectional study of faecal shedding of Giardia duodenalls and Cryptospondium parvum among packstock Jn the Sierra Nevada Range. Equine Vet J 32.247-52, 2000 Cole DJ, Choen ND, Snowden K, et al: Prevalence of and nsk factors for fecal shedding of Cryptosporidium parvum oocysts in horses. J Am Vet Med Assoc 213:1296-1302, 1998
BIOTERRORISM AND EQUIDS
41. Whltlock RH, Buckley C: Botuhsm. Vet Clln North Am Equine Pract 13:107-128, 1997 42. AVMA Council on Biologic and Therapeutic Agents: Guidelines for vaccination of horses. J Am Vet Med Assoc 207:426-431, 1995 43. Keeneiand: Sales Results: Past Sales Summaries. Accessed Feb 5, 2002. URL: http://www.keeneland.com/hvesales/summarles.asp 44. Timoney PJ: Factors influencing the international spread of equine diseases. Vet Chn North Am 16:537-551,2000 45. Apatow SM: Impact of the foot and mouth epidemic on the equestrian industry in the UK - - A reference point for the United States. Humanitarian Resource Institute Biodefense Reference Library (HRIBRL) D~scussion Paper FMDEI-2001-12. Carson City, NV, Human~tanan Resource Institute, 2001 46. United States Animal Health Association: Foreign Animal Diseases. Richmond, VA, Carter Printing Company, 1998 47. Nolen RS: Veterinarians key to d~scoverlng outbreak of exotic encephalitis. J Am Vet Med Assoc 215:1415-1419, 1999 48. Preslar DP: The role of disease surveillance in the watch for agroterrorism or economic sabotage. Accessed Jan 3, 2002. URL: http:// www.fas.org/ahead/bwconcerns/agroterror.htm 49. Noah DL, Sobel AL, Ostroff SM, et al: Biological warfare training: Infectious disease outbreak differentiation criteria. Mil Med 163:198201, 1998 50. Paviln JA: Epidemlology of bloterrorism. Emerg Infect Dis 5:528-530, 1999 51. United States General Accounting Office: Vulnerability of crops and hvestock to a biological attack. Washington, DC, United States General Accounting Office, May 1998, Report No. GAO/C-RCED98-1
115
A bioterrorism attack can affect the health of many different populations, even those that were not intended as targets. Whether the aim of an attack ts humans, antmals or crops, the result can be mantfested in many species, including equids. Equlds comprise a multibilhon-dollar industry in the United States, and any disease that affects this trade can have a devastating impact on the economy. In addition, equids could potentially serve as sentinels of an attack against humans, or as amphfymg hosts for certain diseases. Knowledge of what diseases have the greatest potential as bioterronst or agroterronst agents, how they may present, and what preventive measures are needed to stop their spread is the first step in preparedness. Surveillance for disease outbreaks in equids should be ongoing, with immediate reporting of any unusual findings to the appropriate veterinary and public health authorities. Key words: BIoterrorism, veterinary public health, equlds. Copyright 2002, Elsevier Science (USA). All rights reserved.
he recent biological attacks in the United States revealed
T vulnerabilities that we did not anticipate. Prior to Novem-
ber, 2001, many scientists and health professionals did not appreciate the ability of dried spores of Bacillus anthracis to permeate envelopes and spread throughout buildings and infect people via both the cutaneous and inhalational routes. The need to protect workers against such a threat had not been previously considered. For most of the US population, the need to prevent and respond to a bioterrorist attack against our agricultural industry and the equine population in particular had also not been realized, much less appreciated. The threat of agroterror]sm or an attack against the nation's agroindustries ]s not theoretical. Eleven documented incidents of biological warfare, terrorism, or crimes perpetrated against animals have occurred in the 20th century, 6 of them involwng eqmds. 1 In the wake of September 11 th and the anthrax letter attacks, the threat of an act of agroterrorism has assumed much greater importance for both the human and veterinary health communities. On 11 September, the US Department of Agriculture's (USDA) Animal and Plant Health Inspection Service (APHIS) issued a statement emphasizing the need to increase Foreign Animal Disease (FAD) surveillance nationwide.2 The American Veterinary Medical Association's president, Dr James H. Brandt, also highlighted the vulnerabdity of the nation's livestock populations to the introduction of foreign diseases via an
From the Department of Defense Global Emerging Infections System, Walter Reed Army Insbtute of Research, Silver Spnng, MD. Address reprint requests to LTC Julie Pavlln, Division of Preventive Medtcine, Walter ReedArmy Institute of Research, 503 Robert Grant Ave, Silver Spring, MD 20910-7100. Copyright 2002, Elsevier Science (USA). All rights reserved. 1534-7516/02/0102-0000535.00/0 dol:l 0.1053/ctep.2002.34239
act of agroterrorism in a letter to Tom Ridge, Secretary of Homeland Defense. 3 Since its initial discovery in North America in 1999, West Nile virus provides an important example of the abihty of a newly introduced pathogen to spread quickly in the United States. 4 Medical professionals caring for any species need to be increasingly vigilant in helping to prevent, detect, or, if it occurs, treat the victims of a bioterrorist attack. The value of the livestock and poultry industries in the United States is estimated at $50-200 bilhon, with over $50 billion in annual exports. 35 Agriculture is also the largest sector of the US economy, representing 13.3% of the Gross National Product (GNP). 6 The nation's livestock population is also highly susceptible to a range of important FADs. A highly contagious and virulent infectious disease such as foot-and-mouth could wreak economic havoc with losses estimated to exceed $30 billion. 5 In addressing the potential impact that certain exotic diseases could have on the equine population in the United States, consideration should be given to the current significance of the horse industry to the national economy. This is frequently grossly underestimated and seldom fully appreciated. The most recent national study undertaken was for the tax year 1994 and examined the diversity of the industry, with specific regard to the activities that contribute directly to the production of horses or that provide amusement and recreation services involving horses, r Based on an estimated population of 6.9 million equids in the United States and approximately 7.1 million human participants, the goods and services produced by the horse industry were valued at $25.3 billion. It contributed as much as $112.1 billion in gross domestic product and provided an estimated 1,404,400 full-time equivalent jobs. The annual revenue from the sale of horses, ponies, and other equids in the United States has continued to increase, especially in recent years, and is currently close to $2 billion. Before the terrorist attacks on the United States, USDAAPHIS developed a National Emerging Response Program to a Highly Contagious Animal Disease for the United States in partnership with the American Vetermary Me&cal Association, the US Animal Health Association (USAHA) and the National Institute for Animal Agriculture (NIAA). The goal of the program was to assist in education, surveillance, prevention, and response to an agroterrorist attack. 8 However, a survey carried out m 2000 by the Minnesota Department of Health to determine veterinary surveillance capacity for zoonotic bioterrorist agents revealed that some high-priority organisms such as plague and tularemia are not reportable diseases in all states, that 39% of state animal health officials had not been involved in bioterrorist or agroterrorist planning and coordination, and that few efforts to educate veterinarians on bioterrorist Issues had been instituted. 9 The first line of defense agamst bioterrorism is a force of educated professionals who can, in the event of
Clinical Techniques m Equine Practice, Vol 1, No 2 (June), 2002: pp 109-115
109
an attack, recognize the signs of a disease and assist with surveillance and response efforts. This article outlines the classification of agents of potential btoterrorist or agroterrorist importance, describes the most significant threats to the equine population, discusses the potential impact on the equine industry and the national economy, and provides an overview of appropriate surveillance measures.
Category
Agent
A
Agents of Bioterrorist or Agroterrorist Potential
B
Vanola major (smallpox) Bacillus anthracis (anthrax)* Yersmia pestls (plague) Clostridlum botulinum toxin (botuhsm)* Franclsella tularensis (tularemia)* Filovtruses (eg, Ebola and Marburg) Arenavtruses (eg, Lassa and Junto) Coxlella burnetti (Q fever) Brucella species (brucellosis)* Burkholderia mallei (glanders)* Alphaviruses (eg, Venezuelan, eastern, and western encephalitis)* Rtcm toxin from Ricinus communis (castor bean)* Clostndium perfnngens toxin* Food and water-borne pathogens (eg Salmonella species,* Shigella dysentenae, Escherichla coli O157:H7, Vibrio cholerae, and Cryptospondlum parvum) Nipah virus* Hantawruses Tmkborne hemorrhagic fever wruses Ttckborne encephahtls virus* Yellow fever Multidrug-reststant tuberculosis
Biological terrorism is the use of a microorganism, toxin, or bioregulator derived from a living organism to cause death or disease in people, animals, or plants. More recently, the term agroterrorism has been applied to situations involving animals or plants. Compared with various human pathogens that may require special manipulations before they can be used effectively as biological weapons, animal pathogens, including some of equine importance, could be employed without undergoing any prior treatment. Many of the pathogens on the list of potential agroterrorist agents may be responsible for natural outbreaks of disease. It is important, therefore, to differentiate between a natural outbreak of a disease and a disease occurrence resulting from the deliberate introduction of a particular agent or toxin, even though the strategies for treatment and prevention of spread may not differ in either situation. Animals could be the targets of a biological attack, or they could serve as sentinels of a bioterrorist attack directed against humans. After the accidental release of Bacillus anthrac~s spores in a military facility in Sverdlovsk, USSR, in 1979, human cases of disease were reported 4 km downwind of the facility, whereas deaths in sheep and 1 cow due to anthrax were recorded 50 km downwind. 1° Regardless of the intended target° a disease agent may cause significant morbidity and mortality in a susceptible animal population, and, in the case of certain diseases such as Venezuelan equine encephalomyelitis (VEE), amphfication of the disease through animals poses an increased threat to humans. During the Cold War, biological weaponry programs in many countries were focused on agents that had high toxicity or pathogenicity, were easy to produce in bulk, and were stable in the environment or under conventional storage conditions. Irrespective of what approach was taken, most countries developed a similar prioritized list of agents. Of these, B. anthracis, Brucella suis, Coxiella burnetii, the equine encephalomyelitis viruses, and various other arboviruses can cause disease in equids. 11 In addition, toxins such as botulinum toxin and ricin can also cause morbidity and mortality in equids. In 2000 the Centers for Disease Control and Prevention (CDC) issued a plan for preparedness and response to biological and chemical terrorism. ~2 To conserve resources, they recommended targeting preparation activities against certain highly significant biological agents Some biological agents are deemed more critical than others based on how high a risk they pose to nauonal security. The criteria used for evaluation include: 1) how easily the agent can be disseminated or transmitted person-to-person; 2) the potential of an agent to cause high mortality and have a major public health impact; 3) the ability of the agent to cause public panic and social disruption; and 4) whether the agent would require special action for public health preparedness.S"- In the case of an agroterrorist attack that affects animals primarily, or as a secondary consequence of airborne or other means of widespread dissemination, we be1 10
TABLE 1. CDC List of Critical Biological Agents
C
NOTE List from Centers for Dtsease Control and Prevention (CDC). 12 *Disease agents that can cause dtsease in equtds.
lieve that an additional criterion, economic impact, should also be considered when prioritizing preparative activities to deal with such an event. The CDC priorttizes biological agents into 3 categories--A, B, and C--with A posing the greatest threat. The biological agents considered critical by the CDC are listed in Table 1. Smallpox and plague are among the diseases posing the highest risk threats to humans, neither of which are pathogenic for equids. However, other infectious agents such as Hendra virus, vesicular stomatitis virus, and African horsesickness virus are threats to equine health. Using the same criteria as the CDC but including the economic impact of a disease, we have compiled a prioritized threat list for equids (Tables 2, 3, and 4). Clearly, some of these agents are zoonotic and if introduced into the United States could spread to human populations. Other agents, such as dengue virus, Congo-Crimean hemorrhagic fever virus and Shigella spp that do not cause disease in equids should still be of concern because seroconversion or isolation of these disease agents in equtds has been documented. 19
Impact of Bioinvasions on the Horse Industry in light of the considerable economic importance of the US horse industry, it is not difficult to appreciate the tremendous financial impact certain exotic diseases could have were they to be introduced into the country's highly susceptible equine population. How significant an impact a particular disease would have depends not only on the particular infectious agent and its primary route(s) of transmission, but also on the activity category of the horse industry that is principally involved. In the most recent economic impact study of the US horse industry, horses and participants in the industry were categorized into 4 groups by activity--racing, showing, recreation, and other (farm and ranch work, police work, rodeo, polo, and so on). Contributions of each of these categories to the Gross Domestic Product total of $112.1 billion in 1994 were 29% each for racing and showing, 27% for recreation, and the other equine activities accounting for the remaining 15%7 PAVLIN ET AL
TABLE 2. Viral Agents With Potential Agroterrorist Significance for Equids
Agent; Zoonot~c Status
Mode of Exposure*
African horse s~ckness¶ (13-15)
IVn (13,16) IHa p~
D~rect Transmission Expected Case Economic Potential m a Fatality Rate m Likely Agent Occurs Impact on Agroterronsm Clinical Equ~ds From Agroterronst Naturally in Equine Event; H, Between Presentation Agroterronst Potential1the US? Industry:l: Horses; M, to Man m Equ~ds§ Event
Control Measuresll
Unlisted
No#
HNh
H, no; M, no
RL (acute), CV (chronic)
Eastern equine IVan (16), IHa encephalomyeht~s wrus** (16-18) Japanese IVn (16) encephaht~s wrus¶,** (13,19) Venezuelan equine IVan (16), IHan encephalomyeht~s v~rus¶,** (13,17,18)
B, E
Yes,l-i late summer to fall No# (13)
Moderate
H, no; M, no
FE, NE
H~gh, VC, V, I, E, especially for DC pulmonary form H~gh VC, V
Low
H, no; M, no
UA, NE
Low
V
H~gh
H, yes:l:$; M, yes$$
FE, NE
H~gh
PP, VC, V, I
Western equine encephalomyelitis wrus** (16,17)
IVan (16); IHa (17)
B, E
Moderate
H, no; M, no
FE, NE
Moderate to h~gh
VC, V
West Nile fever wrus** (20-23) Hendra wrus¶,** (24-26) Influenza A virus¶,** (16) Rotavlruses** (27) T~ckborne encephaht~s wrus, Iouping ill¶,** (16,18) Vesicular stomatlt~s** (13 14,29,30)
IVa n (16)
Unhsted
Yes, southern and tropical US; rainy season Yes, western and central US, summer to fall Yes§§
H~gh
H, no; M, no
UA, NE
VC, V
IHan IIII IG a ~ II[I IHa,7
C
No#
H~gh
H, yes¶¶; M, yesllll
FE, RL, NE
Moderate to h~gh High
D, E
Yes, sporadic Moderate
H, yes; M, yes
Yes No#
Low Moderate
H, yes; M, yes H, no; M, no (18)
FE, RU, RL, DE DI FE, NE, UA (28)
Yes, especially V, I in foals Low S, V, I Possibly high PP, VC (18,28)
Yes
Moderate
H. yes##; M, yes##
FE, VE
Low
Unhsted B, D, E
IGan D IV~ (28), SC,~ C, D IH,~ ~ P~ (w~th ~nfect~ve blood) IVn (13), Unlisted phlebotomine fly (18), IHa*, SCa?
S, E?, I
VC, V?, I
NOTE. C~tat~onsto references are in parentheses. %, agroterrorism; n, natural; IG, ingestion, pnmarily due to food and water contamination; IH, inhalation of aerosohzed agent; IV, insect vector (T, tick; M, mosquito; F, fly); P, parenteral, through rejection, implantation etc; SC, skin contact, including mucus membrane contact, usually thought to require broken skin. 1-CDC classification as per (12): A, top pnonty agent; B, second level pnority agent; C, tNrd level priority agent, D, known to have been weaponized or under development as a btoterronsm weapon in the past (6); E, c~ted as potential biological terronsm agents (12). SPresumed impact based on 5 cntena (assessment of combination of transmission potential, seventy of disease, public fear, need for special measures, and economic and trade disruption). §AB, abortion; AD, lymphadenopathy (w~th or without ulceration); AN, anorexia; FB, fistulous bursitis; FE, fever; CV, cardiovascular (hypotension, shock, heart failure, cardiac arrest, etc), DE, depression; DI, diarrhea; DB, debilitation; GI, gastrointestinal including cohc; HE, hemorrhage; IM, ~mmunosuppressJon, NE, neurologJc; NU, nodular-ulcerative (abscesses, cutaneous, respiratory etc); NT, necrosis topical; RL, lower respiratory; RU, upper respiratory; SE, septicemia; SP, symmetncal descending flaccid paralys~s; UA, unapparent or asymptomatlc; VE, vesicles. IIAssumptlon of transmission potential: A, antlm~croblals; AT, antitoxin; DC, stnngent decontamination of stable/environment; E, euthanasia/ ehminatlon of infected animal; i, ~solatlon/quarantine; PP, use of personal protectwe precauttons such as gloves, gowns, mucus membrane protection; S, basic sanitation; V, vaccnat~on; VC, vector control; W, clean water supply (water borne diseases). ¶Foreign animal disease (14). #Not seen in the US unless imported. **Disease considered zoonotlc (14). 1-1-in eastern and gulf states; less common than western equine encephalitis or St Louis encephahtis, but more serious in humans (16). $:l:Mechanlcal transmission via biting insects possible (16); direct via aerosol possible (13). §§Recent introduction into the US presumed to be naturally occurring. IIIISuspected but not definitive, role of flying fox spp (25). ¶¶D~rect and very close contact w~th respiratory secretions of infected animals (humans?) believed to be required (26). ##Exposure to vesicular fluids.
O[ all the exotm &seases that could threaten the health and economic well-being of the US horse industry, African horsesmkness and VEE, both vector-borne diseases, have the potential to cause the most serious and devastating epidemics of disease among all categories of eqmds, irrespecuve of use or activity. Furthermore, both diseases would drastically impact the ability of the US to export equids or equine semen throughout the world. An example of how sigmficant this export trade has become, especially in the past 5 to 10 years, can be gauged from the fact that approximately one third of the total sum realized at the world-renowned Keeneland Sales m Kentucky for each of the past 2 years represented overseas purchases, most of which were exported. 43 An inability to maintain this BIOTERRORISM AND EQUIDS
export trade would have major economic repercussions for the horse industry wlth losses in revenue running into several hundreds of millions of dollars per year. The introduction of a highly contagious respiratory-borne pathogen such as a virulent variant of equine influenza virus could have a huge impact on the US racing and show industries. Historically, equine influenza has been responsible for major epidemics wherever the virus has been introduced into previously unexposed and lmmunologically naive populations of equids. The epidemms in South Africa and Hong Kong in 1986 and 1992, respectively, closed down racing m each country for a period of up to 1 to 4 months and resulted m considerable finanmal losses totahng many milhons of dollars. 4~ A similar 111
TABLE 3. Bacterial and Protozoal Agents With Potential Agroterrorist Significance for Equids
Dkely Agroterrenst Potentiali-
Agent Occurs Naturally m the US?
Economic Impact on Equine Industry:l:
Direct Transmission Potential in a Agroterrorism Event; H, Between Horses; M, to Man
Clinical Presentation in Equtds§
Expected Case Fatahty Rate m Equlds From a Agroterronsm Event
H, yes**; M, yes**
rE, RL, NU, GI, HE
Htgh without treatment
A, DC, V?
Moderate
H, yes; M, yes
FB, AB
Unknown, probably low to moderate
A, S, I?
No$:i:
High
H, yes; M, yes
DB, NU
A?, E? I?, DC, PP
SC,~ n D IH,. n IG ~ ~
No:I:~
High
H, yes; M, yes
rE, SE, DB, NU
IG," ~ IH ~
B, D, E
Yes
High especially if resistant
H, yes; M, yes
DI, GI, AB
Moderate to Ngh, chronic carners possible Moderate to high, chronic carriers possible Moderate to high (speciesdependent)
IVn (16), IH, ~
A, D
Yes, In western US
High for H, yes**; M, yes** pneumontc form
rE, AN, DE, RU, DI, AD
Possibly low
B
Yes
Moderate
UA, DI
Low
Agent; Zoonottc Status
Mode of Exposure*
Anthrax (Bacillus
IG, ~n IH, ~ ~ SC ~ IG ~ IH, a ~ SC ~ ~
A, D, E
Yes#
High
B E
Yes
IG,~,~IH~
B, D, E
anthracls) (13,17,31,32) Brucellos~sl]
(Brucella, primarily B
Control MeasuresLI
abortus) t t (16,33) Glanders¶,$$
(Burkholdena malleO (13,17,34) Mellotdosls¶,$:l:
(Burkholdena pseudomallel) (13,16,17) Salmonellosts¶ (Salmonella spp) (13,35,36)
A?, Eg, I?, DC, PP A, I, DC, PP
(16) Tularemia¶
(Franctsella tularensls) (13,37) Cryptospondtosls¶
(Cryptospond/um parvum)
SC, ~ ~ IG~ n IG~ ~
H, yes; M, yes
A, VC, S, PP (for pneumontc) I? A (under investigation), W, S
(38,39,40) *,l-,:]:,§dISymbols and notes as in Table 2. 1]Disease considered zoonottc (14). #Areas of the US w~th neutral or alkaline, calcareous soils can be endemm. **Possible if contact with blood or contaminated animals or carcasses. t~rBrucella spp commonly associated with horses are B abortus and B suls. Brucella spp assoctated wtth b~oterronsm potential are B mefitensis and B suis (17,33) :[:$Forelgn animal disease (14). NOTE. Citations to references are in parentheses.
scenario would likely occur m the United States, given the introduction of a strain of influenza virus against which the country's equine population had not been prevmusly protected. Contagious equine metntis is an example of a contagious, venereally transmissible disease of equids that is currently exotic to the equine population m the Umted States. Were it to be
introduced through an act of agroterronsm, contagious equine metritis could readily spread among mares and stallions and cause major &sruption in the principal centers of horse breeding in the country. It would lead to suspension of breeding operations, restricuon of ammal movement, and considerable financial losses for the horse industry. The inadvertent mtro-
TABLE 4. Toxins With Potential Agroterrorist Significance for Equids
Agent; Zoonotic Status
Mode of Exposure*
Botulism toxin (from
IG, an SC~ IH a
Clostridium botuhnum) (13,17,41 ) Epsilon toxin (from
Economic Impact on Equine Industry:i:
Direct Transmission Potential in a Agroterronsm Event, H, Between Horses, M, to Man
Chn~cal Presentation in Equlds§
H, no; M, no
SP
Likely Agroterronst Potential1
Agent Occurs Naturally in the US
A, D, E
Yes, serotypes B and C most common
Moderate
n
Ricinus communls,
B "~, E?, D
IG, an IH ~
B, D, E
Yes
Moderate
H, no; M, no
GI, RU
D, E
Yes
Moderate
H, no; M, no
NT, IM, NE, CV
pa
castor bean) (13,17)
Trichothecene mycotoxln
IG, "n IH, a pa
Control Measures}l
High in u nvacctnated animals
AT (42)
IG, low; IH, high; P, high
PP
Highly toxic I n horses
IG?, P?
Clostndlum perfnngen ) Rtctn (from
Expected Case Fatality Rate ~n Equlds From a Agroterrorism Event
(-1-2, "yellow ram") (17) NOTE. Citations to references are m parentheses * 1-,$,§,llSymbols and notes as in Table 2.
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PAVLIN ET AL
duction of contagious equine metritis into the thoroughbred breeding industry in Kentucky m 1978 resulted in an estimated direct loss of $4 million at the time. 44 If the disease were to be reintroduced, either accidentally or through an act of agroterronsm, the economic consequences of such an incursion would be considerably greater in today's world of elevated horse values and higher operational costs and would probably exceed $100 million Apart from the direct economic losses that would ensue from the clinical consequences of certain exotic diseases affecting the US horse population, there would be additional financial losses from denied or restricted export markets. If equine diseases currently exotic to this country were introduced through an act of agroterronsm, it would result in major restrictions on trade in horses and equine semen. Aside from the previously cited examples of African horsesmkness, VEE, or contagious equine metritis, other diseases such as vesmular stomatitis, because of its clinical similarity to foot-and-mouth disease (FMD), would adversely affect the industry's ability to trade internationally until the disease had been effectively controlled. In terms of financial significance, if vesicular stomatitis had occurred in Kentucky in 2001, it would have resulted in a &month ban on the export of horses to countries in the European Union and would have led to an estimated loss of over $125 million. 44 There is a general appreciation of the economic losses that would be directly attributable to the deliberate introduction of a specific equine disease such as African horsesickness or VEE. What is not often recognized, however, is that the US horse industry could also suffer very considerable financial damage if another hvestock species besides equids were the target of the exouc pathogen. This was dramatically illustrated by the devastating impact that the large-scale epidemic of FMD in the United Kingdom had on that country's equine industry. 45 Shortly after the disease was confirmed in February, 2001, essentially all horse racing, showing, and recreational activity was banned for several weeks. Racing and certain other equestrian activities later resumed under very stringent conditions involving controlling movements and the observance of strict disinfection measures. However, eventing, hunting, recreational riding, endurance, and point-to-pointing were suspended for many months while the epidemic continued. Large areas of the countryside were closed to horses. The financial impact of these control measures was felt across the industry. Losses were estimated at over $141 million per month from March through May, 2001. There is little doubt that if FMD were deliberately Introduced into the United States, the direct, indirect, and induced effects of the disease on the horse industry would far exceed those experienced during the 2001 epidemic in the United Kingdom. The impact would be felt at all levels of the industry and could result in significant restrictions on international trade in horses and semen.
Bioterrorism Surveillance and Reporting Commensurate with an enhanced awareness and perception of the risk of bioterrorism or agroterrorism, recognition of the need for improved &sease surveillance has also increased. It is worth considering the potential role of equids in any surveillance program for bioterrorism, regardless of the target species, and the factors that can help to differentiate between natural and intentional disease outbreaks. BIOTERRORISM AND EQUIDS
Outbreaks of certain diseases among equine populations have served as sentinel events for the threat of those diseases for humans. Notable examples include various arthropod-borne encephaliudes such as Japanese encephalitis and VEE. In the case of Japanese encephalitis, because humans and equids are both final hosts, horses infected with the virus do not provide a source of infection for humans. However, in temperate Asia, cases among equids typically precede those in people by at least several weeks. 46 Horses also serve as sentinels for human mfeclions in VEE, but for different reasons. In contrast to the other equine encephalomyelitides, equids infected with VEE virus (subtypes lAB or 1C) develop high viremias and serve as very efficient amplifying hosts of the virus. In consequence, they play an extremely important role in propagating an epidemic of the disease in humans. ~6 Recognition of cases of VEE among equine populations is epidemiologically crincal to identifymg the frequency and geographic distribution of infection with this virus, is Equids are of limited potential as sentinel animals with respect to the &seases most likely to be employed by bioterrorists targeting human populations. Although horses are susceptible to a number of these disease agents, such as B anthracls, Burkholderia malle~, Brucella abortus, Coxiella burnetii, and Burkholderia pseudomallei, the low infection rates and similar incubation periods in horses relative to those in humans, make equids unlikely candidates as sentinels. The first recognitmn of West Nile virus in the United States in 1999 is a case in point. Although certain species of birds, ie, members of the corvid family, were identified as potenually valuable sentinels of the risk of exposure of humans, the initial cases among horses on Long Island, New York, occurred either simultaneous with or after reported human cases. 47 Although the equine cases did not qualify as sentinel events, they do serve to illustrate that the manifestation of a newly introduced disease into a susceptible population may be recognized more easily when animal and human health care practitioners communicate on a frequent basis. Once a disease outbreak ~s recognized, an initial question that should be addressed is whether its origins were natural or intentional. Although the point past which epldemiologic proof becomes legal proof is debatable, 4s a number of guidelines have been put forward that can help differentiate between natural and intentional disease events. 49 50 Among those relevant for animal populations are number of cases, temporal patterns of &sease onset (epidemic curve characteristics), clinical presentation, strain or varmnt of etiologic agent, economic impact, geographic location, morbidity and mortality rate, antimicrobial resistance patterns, seasonal distribution, route of exposure, weather and climate considerations, and concurrence with belligerent activities of potential adversaries. Regardless of the causation of the event, rapid reporting must be accomplished for a response to be effective. Whether the veterinarian, owner, or farm manager initially recognizes the disease, prompt notification must be made to the appropriate authorities. Ideally, the veterinary practitioner should notify the state veterinarian and area federal veterinarian-m-charge. Alternatively, an outbreak of an exotic or new disease may be discovered when clinical necropsy specimens are submitted to a veterinary diagnostic laboratory. Evidence or suspicion that the disease is zoonotic should also involve notification of local and state health departments. Upon notification, epidemiologists and diagnosticians may be deployed to assist local investigators in determining the cause of the epidemic and propose an appropriate course of action to bnng it under control. 1 13
Reporting a potential outbreak of a foreign ammal disease should be camed out with a minimum of delay and should include as much information as possible of the circumstances and nature of the occurrence. The responsibility of information generation and reporting should be a shared responslbihty among the local veterinary practitioner, the state veterinarian, the federal veterinarian-in-charge, and the responding foreign animal disease diagnostician. Where indicated, additional reporting to other state and federal agriculture and health officials will be the responsibility of the state department of agriculture. Informatmn provided should include:
3.
4.
5. 6.
7.
• Complete names and addresses of all farms with affected animals. This should include longitude and latitude informatton as well as the type of operation (eg, breeding, racing, boarding). • The same information for potentially exposed ammals on other farms with contiguous fencing that allows face-to-face contact. • Total numbers of animals, including all species, on these farms. Of that total, how many are affected? -What was the date of onset of the first case? Since that tune, how many others have been affected and where were they located or housed in relation to the index case(s)? • Have any affected animals died? If so, what was the disposition of the carcass? Necropsy summary should include descriptions of the body, skin, head area, respiratory system, cardiovascular system, digestive tract/abdominal cavity, urogenital tract, musculoskeletal system, nervous system, and lymph nodes. • Have laboratory samples been taken and submitted? If so, what samples, how many, and where and when were they sent? • Animal movement history. Were affected animals moved anywhere in the few months preceding this event? If so, where and when? Were other animals on the premises moved during the same period? If so, where and when? • Have there been any reports of associated human Illness among farm owners or staff? • Complete physical examination results of affected animals. This should include descriptions of the body (including temperature, behavior, gait, condition, and general appearance), skin, head area, respiratory tract, cardiovascular system, digestive tract and abdomen, urogenital system, musculoskeletal system, nervous system, and lymph nodes. • Finally, an initial list of differential climcal diagnoses should be included. Only when agricultural commodities such as horses, other livestock species, and even crops are included in national survetllance networks, will the United States be able to recognize and respond to natural and intentional disease outbreaks in a timely fashion. This will require improved veterinarian-physician communication and enhanced ammal disease surveillance and reporting programs. 48 5~
References 1. W~lson TM, Gregg DA, K~ng DJ, et al: Agroterronsm, biological cnmes, and blowarfare targeting animal agriculture. The chnlcal, pathologic, diagnostic, and epidemlologic features of some important antmal diseases. Clin Lab Med 21:549-591, 2001 2. USDA/APHIS: Foreign animal d~sease surveillance increased. Sep1 14
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BIOTERRORISM AND EQUIDS
41. Whltlock RH, Buckley C: Botuhsm. Vet Clln North Am Equine Pract 13:107-128, 1997 42. AVMA Council on Biologic and Therapeutic Agents: Guidelines for vaccination of horses. J Am Vet Med Assoc 207:426-431, 1995 43. Keeneiand: Sales Results: Past Sales Summaries. Accessed Feb 5, 2002. URL: http://www.keeneland.com/hvesales/summarles.asp 44. Timoney PJ: Factors influencing the international spread of equine diseases. Vet Chn North Am 16:537-551,2000 45. Apatow SM: Impact of the foot and mouth epidemic on the equestrian industry in the UK - - A reference point for the United States. Humanitarian Resource Institute Biodefense Reference Library (HRIBRL) D~scussion Paper FMDEI-2001-12. Carson City, NV, Human~tanan Resource Institute, 2001 46. United States Animal Health Association: Foreign Animal Diseases. Richmond, VA, Carter Printing Company, 1998 47. Nolen RS: Veterinarians key to d~scoverlng outbreak of exotic encephalitis. J Am Vet Med Assoc 215:1415-1419, 1999 48. Preslar DP: The role of disease surveillance in the watch for agroterrorism or economic sabotage. Accessed Jan 3, 2002. URL: http:// www.fas.org/ahead/bwconcerns/agroterror.htm 49. Noah DL, Sobel AL, Ostroff SM, et al: Biological warfare training: Infectious disease outbreak differentiation criteria. Mil Med 163:198201, 1998 50. Paviln JA: Epidemlology of bloterrorism. Emerg Infect Dis 5:528-530, 1999 51. United States General Accounting Office: Vulnerability of crops and hvestock to a biological attack. Washington, DC, United States General Accounting Office, May 1998, Report No. GAO/C-RCED98-1
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