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Introduction of a foreign animal disease into coun-tries previously free of the disease has resulted in

substantial negative economic consequences for those countries.1-4 The costs of recent classical swine fever outbreaks in The Netherlands and Germany have been estimated at > $2 billion (US currency),3,5-7 and the FMD outbreak in the United Kingdom in 2001 report-edly cost > £3 billion.8 Similarly substantive economic losses, $6.8 to $14 billion or more, have been project-ed in the instance of an FMD outbreak in the United States.9,10 In addition to direct costs of containment and eradication,3 substantial concern exists for the poten-tial impacts of foreign animal diseases on international trade and animal and human welfare.4,11,12

Swine are susceptible to many important foreign animal diseases, including FMD and classical swine fever. For this reason, routine surveillance of swine is conducted in Panama to ensure prompt detection of foreign vesicular diseases.13 In addition, swine may be fed food waste, a risk factor for introduction of foreign animal disease that is unique to the species. Improperly cooked food waste fed to swine could contain material

Results of a survey of owners of miniature swine to characterize husbandry practices

affecting risks of foreign animal disease

Edith S. Marshall, dvm, mpvm; Tim E. Carpenter, phd; Mark C. Thurmond, dvm, phd

From the Center for Animal Disease Modeling and Surveillance, School of Veterinary Medicine, University of California, Davis, CA 95616.

Supported by a contract with the California Department of Food and Agriculture and funds from the Department of Homeland Security and the National Center for Foreign Animal and Zoonotic Disease Defense.

The authors thank the California Potbellied Pig Association and the Southern California Association of Miniature and Potbellied Pigs.

Address correspondence to Dr. Marshall.

Objective—Tocharacterizehusbandrypracticesthatcouldaffecttherisksofforeignanimaldiseaseinminiatureswine.Design—Surveystudy.Study Population—106ownersofminiatureswine.Procedures—An online survey of owners of miniature swine was conducted to obtaininformationaboutminiaturepigandownerdemographics;pighusbandry;movementsofpigs;andpigcontactswithhumans,otherminiatureswine,andlivestock.Results—12states,106premises,and317miniatureswinewererepresentedinthesur-vey.Morethanathird(35%)ofminiatureswineownersalsoownedotherlivestockspecies.Regularcontactwithlivestockspeciesatotherpremiseswasreportedby13%ofowners.Morethanathirdofownersvisitedshowsorfairs(39%)andcluborassociationevents(37%)whereminiatureswinewerepresent.Morethan40%ofownersfedfoodwastetominiatureswine.Approximatelyhalf (48%)of theveterinariansprovidinghealthcare forminiatureswinewereinmixed-animalpractice.Conclusionsand Clinical Relevance—Resultsofthisstudyindicatedthatminiatureswinekeptaspetscanbeexposed,directlyandindirectly,tofeedandotherlivestock,potentiallyintroducing,establishing,orspreadingaforeignanimaldiseasesuchasfoot-and-mouthdis-ease.Inaddition,theveterinaryservicesandcarcassdisposalmethodsusedbyminiatureswineownersmayreducethelikelihoodofsickordeadpigsundergoingante-orpostmor-temexaminationbyaveterinarian.(J Am Vet Med Assoc2007;230:702–707)

AbbreviAtion

FMD Foot-and-mouthdisease

contaminated with FMD or other agents and is believed to be the source of infection for a swill-feeding swine operation that was the index case in the 2001 UK out-break of FMD.14 Several other foreign animal disease outbreaks have been attributed to food waste feeding of swine, including outbreaks of African swine fever in Belgium in 1985, classical swine fever in several Eu-ropean countries from 1986 through 1995, and swine vesicular disease in the United Kingdom from 1972 through 1980.15,16 Because of their disease susceptibil-ity and historical role in outbreaks, swine should be considered to be a subpopulation of livestock at high risk for the introduction and transmission of FMD in the United States.

Miniature swine are not typically raised in com-mercial swine production husbandry and management environments. Instead, they may be kept as household or backyard pets and fed table scraps or other food waste that could increase the risk of foreign animal dis-ease introduction or transmission. The recent incursion of exotic Newcastle disease, a foreign animal disease, into southern California in 2002 emphasized the need to understand the practices used to manage susceptible pet and backyard animal populations.17 Early in the course of the exotic Newcastle disease outbreak, only backyard poultry flocks were found to be infected.18 As the epidemic progressed, the infection was transmitted

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to commercial egg-laying flocks.19 Similarly, depending on feeding and management practices, miniature swine kept as pets could potentially initiate an outbreak, con-tribute to disease transmission, or maintain an epidem-ic of FMD. Although recent attention has been directed at the potential for miniature swine to play a role in foreign animal disease outbreaks,20,21 features of their environments that could affect risk of a foreign animal disease, such as husbandry practices, human and live-stock contacts, and animal movements, have not been described for pet miniature swine. An understanding of how miniature swine are raised and the potential for disease transmission may be particularly important be-cause these animals are kept as pets and may not receive the same degree of veterinary or regulatory supervision as commercial swine herds. It is not known whether an outbreak of FMD could be initiated in this population through risky practices, such as feeding of undercooked food waste, or if transmission to other livestock species would likely occur through direct contacts, indirect contacts, or both. In addition, to the authors’ knowl-edge, no information has been published regarding the extent of veterinary services and carcass disposal meth-ods used by owners of miniature swine, information that would be necessary to yield sufficient oversight or opportunity for diagnosis of a foreign animal disease. The objective of the present study was to characterize husbandry practices that might affect risks of foreign animal disease, specifically FMD, in miniature swine.

Materials and Methods

An online survey of miniature swine owners was un-dertaken to obtain information about the number of pigs owned; food waste feeding; veterinary care; movements on and off the premises; and contacts with humans, oth-er miniature swine, and livestock species. An Internet search revealed associations, individuals, and veterinar-ians linked to miniature swine. Individuals were contact-ed and invited to help distribute the survey to owners of miniature swine. Four hundred individuals received an e-maila explaining the purpose and nature of the survey and giving the Web address of and a link to the online survey. Recipients of these e-mails were asked to com-plete the survey and to encourage other miniature swine owners to do so. In addition, 21 veterinarians working at practices in California that provide services to own-ers of miniature swine were identified. The veterinarians were contacted and asked to invite clients with miniature swine to participate in the survey. A reminder e-mail was sent to organization members a few weeks after the ini-tial survey announcement was e-mailed.

From June 8, 2005, to August 8, 2005, after a 10-day period of pilot testing, the survey format was made avail-able online through a Web-based survey service.b Ques-tions asked had closed-ended, partially open-ended, and open-ended formats. Owners’ ZIP codes and nearest cross street were collected to identify the state and city of prem-ises location. Each respondent was limited to 1 survey sub-mission. No information that would enable identification of an owner was collected or made available to the inves-tigator. Prior to survey distribution, authorization for the study of human subjects was obtained from the university institutional review board (Protocol 200513389-1).

Respondents’ general locations were recorded in a geographic information system software program.c If the nearest intersection to the respondent’s premises was provided, the latitude and longitude of the location were identified by use of the software program’s geore-ferencing tool or through a combination of Web-based mapping services.d-f When only a city or ZIP code was provided, the latitude and longitude of centroid of the city or of the ZIP code region were recorded. To evalu-ate swine movement distances, respondents were asked to identify the city of origin for movements to their premises or destination city for movements from their premises. The latitude and longitude of the centroid of the identified origin or destination city were used. The distance between the movement origin or destination and the respondent’s premises location was calculated. All distances were measured with straight lines between origin and destination locations as opposed to measur-ing the length of the actual routes of travel.

Results

Demographics—After initially contacting 400 miniature swine owners, 106 (26.5%) survey respons-es were collected. Three hundred seventeen miniature swine were accounted for by these owners. Of the 106 respondents, 81 (76%) resided in California. Eighty of those 81 respondents reported owning a total of 257 miniature swine. The remaining respondent from California owned pigs but did not report how many. Respondents were also from New York (n = 2 [2%]), Hawaii (1 [1%]), Florida (5 [5%]), Utah (2 [2%]), Washington (1 [1%]), Virginia (1 [1%]), West Virginia (3 [3%]), Oregon (1 [1%]), Alaska (1 [1%]), Nevada (1 [1%]), and Pennsylvania (2 [2%]). Locations of 5 respondents who did not provide a complete or accu-rate ZIP code could not be identified; data from those records were included only in values reported for the total of all responses. Because the survey responses were predominantly, but not exclusively, from Califor-nia, we reported the data by Californian, non-Califor-nian, and overall responses.

Owners generally kept only 1 or 2 miniature swine (Table 1). A maximum of 39 miniature swine were kept at 1 California premises, which reported rescue or fos-tering as their primary activity. Approximately one third of respondents also owned other livestock. Although ≥ 85% of owners reported keeping miniature swine as family pets, ≥ 33% of miniature pigs were considered to have been rescued or fostered.

Veterinary care and carcass disposal—More than 40% of the veterinarians consulted by miniature swine owners were in mixed-animal practice (Table 2). More than 20% of practitioners treating miniature swine were in small animal practice, and fewer were in large-animal practice. The mean number of veterinary visits per year was approximately 1. In California, > 50% of veterinary examinations of miniature swine occurred at a veterinary clinic; outside of California, examinations occurring at a clinic were reported by 20% of owners. The remainder of veterinary examinations occurred on the owner’s prop-erty or at either location. A small percentage of miniature swine did not receive any veterinary care.

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Table1—SummaryofcharacteristicsofminiatureswineoperationsinasurveyofownersofminiatureswineresidinginCaliforniaandotherstatesin2005.Dataaregivenasproportions,withthesamplenumberasthedenominator.

Respondentstateofresidence

Variable California Non-California Allstates*

No. of pigs owned 80 responses 18 responses 98 responses 1 35/80 6/18 41/98 2 25/80 3/18 28/98 3–5 14/80 6/18 20/98 . 5 6/80 3/18 9/98

Primary function of pigs 79 responses 20 responses 99 responses Family pet 72/79 17/20 89/99 Rescued or fostering 7/79 3/20 10/99

Primary function of pigs 257 pigs described 60 pigs described 317 pigs described Family pet 150/257 40/60 190/317 Rescued or fostering 106/257 20/60 126/317

Other livestock owned 29 responses 7 responses 37 responses Camelids 5/29 1/7 6/37 Cattle 2/29 0 2/37 Goats 13/29 2/7 15/37 Other swine 3/29 0 3/37 Sheep 6/29 1/7 7/37 Other species† 15/29 2/7 18/37

No. of people in direct contact with miniature swine 78 responses 18 responses 96 responses 1 9/78 4/18 14/96 2 30/78 6/18 36/96 3–5 35/78 5/18 41/96 . 5 4/78 3/18 7/96

No. of owners in contact with cloven-hoofed animals at other locations 10 responses 3 responses 14 responses Daily 3/10 1/3 5/14 Weekly 2/10 0/3 2/14 Monthly 3/10 2/3 5/14 Yearly 2/10 0 2/14

Would request necropsy if miniature pig dies 76 responses 17 responses 95 responses Likely 9/76 7/17 16/95 Somewhat likely 14/76 4/17 20/95 Unlikely 53/76 6/17 59/95

*All states includes California, non-California, and data for records in which the state was not identified. †Other species includes horses, mules, donkeys, rabbits, poultry, and species not otherwise listed.

Table2—CharacteristicsofprovidersofveterinarycareforminiatureswineinasurveyofownersofminiatureswineresidinginCaliforniaandotherstatesin2005.

Respondentstateofresidence

Variable California Non-California Allstates*

Regular veterinarian’s practice type 74 owners 17 owners 93 owners Small animal only 20/74 4/17 24/93 Exotics only 1/74 0 1/93 Equine only 1/74 0 1/93 Food animal only 1/74 0 1/93 Large animal only 16/74 1/17 17/93 Companion animal 3/74 1/17 4/93 Mixed animal 32/74 11/17 45/93

No. of veterinary visits per year 81 owners 20 owners 106 owners Mean 1.2 1 1.1 Median 1 1 1

Location of veterinary service provision 75 owners 17 owners 94 owners At veterinary clinic 43/75 3/17 47/94 On owner’s property 12/75 7/17 20/94 Either or both 18/75 6/17 24/94 No treatment 2/75 1/17 3/94

See Table 1 for key.

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Thirty-five percent to 70% of owners reported they were unlikely to request postmortem examination if a miniature pig died (Table 1). More than 40% of own-ers reported that, in the event of a miniature pig’s death, they would bury the carcass on their property (Table 3). Fewer than 12% of owners reported they would have the carcass rendered.

Contacts with humans and other animals—Ap-proximately 50% of all owners indicated that ≥ 3 hu-mans came into contact with their animals (Table 1). Regular contact with cloven-hoofed animals on other premises was reported by 12% (10/18) of owners in California and 15% (3/20) of owners in other states.

For a typical year, ≤ 25% of respondents reported visits to their premises by hay trucks (8/81 [10%] of re-spondents in California; median, 6.3 visits/y; 4/20 [25%] non-California respondents; median, 2 visits/y), feed trucks (2/81 [2%] respondents in California; median, 7.5 visits/y; 1/20 [5%] non-Californian respondents; me-dian, 52 visits/y), animal haulers (5/81 [6%] respondents in California; median, 2 visits/y; 1/20 [5%] non-Califor-nian respondents; median, 6 visits/y), other supply trucks (12/81 [15%] respondents in California; median, 3.5 vis-its/y; 3/20 [15%] non-Californian respondents; median, 6 visits/y), or sales representatives (5/81 [6%] respondents in California; median, 2 visits/y; 1/20 [5%] non-California respondents; median, 3 visits/y). Other miniature swine owners visited respondents’ premises both in California (28/81 [35%]; median, 3.5 visits/y) and outside Califor-nia (6/20 [30%]; median, 5.5 visits/y). Visits to premises by door-to-door delivery service personnel were reported by approximately two thirds (54/81 [67%] respondents in California; median, 12 visits/y; 12/20 [60%] non-Califor-nian respondents; median, 4.5 visits/y) of miniature swine owners. Visitation of the premises by school children or 4-H or Future Farmers of America groups was reported by 44% (36/81; median, 19.5 visits/y) of respondents in Cali-fornia and 35% (7/20; median, 12 visits/y) of non-Califor-nian respondents.

During the past year, ≤ 15% of miniature swine own-ers had visited other cloven-hoofed livestock operations, such as dairies (2/81 [3%] respondents in California; me-dian, 26.5 visits/y; 0/20 non-Californian respondents), beef ranches (2/81 [3%] respondents in California; medi-

an, 26.5 visits/y; 0/20 non-Californian respondents), other (nonminiature) swine operations (3/81 [4%] respondents in California; median, 6 visits/y; 3/20 [15%] non-Califor-nian respondents; median, 10 visits/y), small ruminant premises (5/81 [6%] respondents in California; median, 4 visits/y; 3/20 [15%] non-Californian respondents; median, 12 visits/y), or sales or auction yards (3/81 [4%] respon-dents in California; median, 2 visits/y; 1/20 [5%] non-Cal-ifornian residents; median, 2 visits/y). Approximately 30% of owners reported visiting other premises where miniature swine were kept (23/81 [28%] respondents in California; median, 3 visits/y; 6/20 [30%] non-Californian respondents; median, 8 visits/y). In the previous year, approximately one third of owners attended shows or fairs (32/81 [40%] re-spondents in California; median, 1 visit/y; 6/20 [30%] non-Californian respondents; median, 1.5 visits/y) or miniature swine club or association events where miniature pigs were present (31/81 [38%] respondents in California; median, 2 visits/y; 7/20 [35%] non-Californian respondents; median, 2 visits/y). In California, > 25% of owners attended a min-iature swine club or association event where miniature pigs were not present (23/81 [28%]; median, 2 visits/y). Fewer than 10% of owners outside California attended a similar event (1/20 [5%]; median, 1 visit/y).

Wild deer were observed within 500 feet (152.4 m) of miniature swine on 20% (16/81 respondents; median, 30 observations/y) of premises in California and 25% (5/20 respondents; median, 75 observations/y) of premises out-side California. One owner reported seeing elk near min-iature swine once yearly. Feral pigs were observed daily at 1 premises in Florida.

Food waste feeding practices—Twenty percent (non-California) to 50% (California) of owners report-ed feeding food waste from any source to their minia-ture swine. The most frequently reported source of food waste was the owner’s household (36%). A single owner fed food waste from an industrial source such as a prison or school but did not report feeding meat or dairy waste from this source. Food waste containing meat, dairy products, or both was fed at up to 16% of miniature swine premises. Of those owners who fed any food waste, feed-ing of dairy waste was reported by 33% to 60% of owners and feeding of meat waste was reported by 10% to 20% of California and non-California owners, respectively.

Table3—CarcassdisposalmethodsforminiatureswineinasurveyofownersofminiatureswineresidinginCaliforniaandotherstatesin2005.Foreachproportion,thedenominatoristhenumberofresponses.

Respondentstateofresidence

Carcassdisposalmethod California Non-California Allstates*

Transport to veterinarian 15/81 2/20 18/106Picked up by veterinarian 4/81 2/20 6/106Bury on owner’s property 35/81 11/20 47/106Bury elsewhere 7/81 0 7/106Take to renderer 1/81 0 1/106

Picked up by renderer 9/81 0 9/106Take to dump or landfill 1/81 1/20 2/106Other 19/81 5/20 24/106 Cremation 12 2 14 Contact animal control 4 0 4 Call veterinary hospital 0 2 2 Burn on property 1 0 1 Unsure 2 1 3

See Table 1 for key.

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Animal movement—Of the 3 most recent move-ments of miniature swine from an owner’s premises, > 66% were to visit a veterinarian. At least 60% of move-ments from the premises involved only 1 pig and had taken place in the previous 6 months. Most animal movements from owners’ premises in California involved distances < 50 km (1 way). More than 30% of movements for own-ers outside California involved distances ≥ 100 km.

One-way movements of miniature swine to owners’ premises were most often from the veterinarian, a res-cue or fostering facility, or another private individual. Of the 3 most recent movements of miniature swine to owners’ premises, most involved only 1 or 2 pigs, had taken place in the previous 6 months, or were estimated to have involved distances < 100 km. No movements were reported involving pet or livestock dealers, sales yards, or auctions.

Discussion

Miniature swine owners reported feeding dairy prod-ucts, meat products, or both to pigs, which could lead to the introduction of FMD or another foreign animal disease. Feeding of food waste to swine has been associated with several outbreaks of FMD, classical swine fever, and African swine fever.7,14-16 Miniature swine fed contaminated food waste that has not been adequately cooked prior to feeding could initiate an outbreak of 1 or more of these diseases. It is reported that the risk of transmitting FMD through milk and dairy products is low.22 However, imported meat and meat products have been implicated in the introduction of foreign animal disease outbreaks, including FMD, through food waste feeding of swine.16,17, 23

Delays in FMD diagnosis in miniature swine could lead to disease establishment and transmission to other livestock populations. The present study revealed that min-iature swine may receive veterinary care 1 time/y and that some pigs receive none. In general, veterinary practitioner preparedness for foreign animal diseases has been viewed as critically deficient.24,25 Many owners of miniature swine indicated that their pigs received veterinary care from small animal practitioners, who may not be as alert to or educated about signs of foreign animal diseases as practitioners who regularly deal with livestock species. In the event of a min-iature pig’s death, most owners reported that they would be unlikely to request a necropsy and many would bury the carcass on their property. Under these circumstances, a vet-erinarian would have little opportunity to detect a foreign animal disease that caused a pig’s death.

Disease transmission interfaces between minia-ture swine and other susceptible livestock populations through indirect contacts appeared to be more limited than those that could occur through direct contacts. Most miniature swine owners either did not visit other livestock premises or did so infrequently, indicating a restricted opportunity for disease transmission through human contact. Vehicles and humans who also visit other livestock premises, such as hay and feed trucks, were uncommon visitors to miniature swine premises, suggesting limited indirect contact between miniature swine and other livestock, such as on dairy, beef, and commercial swine operations. Visits by public groups and delivery services were most commonly reported; the risk of disease transmission to other miniature

swine or livestock premises by these types of indirect contacts is unknown but likely to be low. Most owners reported that their veterinarian was a mixed animal prac-titioner, indicating a potential for direct and indirect con-tact with other susceptible livestock species either at the veterinary clinic or through contact with the clinician.

Direct contact of miniature swine with other min-iature swine, livestock, and wildlife could allow for transmission of a foreign animal disease. The results of this study reveal that miniature swine in the surveyed population have opportunities for contact with other miniature swine, wild deer, and other cloven-hoofed livestock that are susceptible to FMD. Movement of miniature swine to or from shows, association events, and rescue facilities could result in disease spread. In California, miniature swine are subject to the same interstate importation regulations as are other swine; however, no intrastate movement regulations apply to these animals.26,g No movements of miniature swine were reported for high–animal-contact livestock en-vironments such as sales yards, auctions, and animal dealers. This finding suggests a limited opportunity for disease transmission to occur from miniature swine to a larger or commercial livestock population through such environments. Rather, transmission may be more likely to occur from miniature swine to other miniature swine and smaller or hobby animal operations via shows, fos-tering environments, and pig-related events.

Because most survey respondents were likely to be affiliated with 1 or more miniature swine associations, they may attend events or shows more frequently than owners who are not affiliated with similar associations. In addition, respondents were contacted via e-mail and completed the survey online. The results of this sur-vey may not be fully representative of miniature swine owners who do not have Internet access or who are not affiliated with miniature swine associations.

Recognizing and describing risk factors for develop-ment of foreign animal disease in miniature swine can aid in assessing the potential for disease introduction, estab-lishment, and transmission both before and during a for-eign animal disease outbreak. In addition to FMD, min-iature swine are also susceptible to infection with viruses that cause classical swine fever,27 African swine fever,28,29 and H5N1 avian influenza.30 Risk factors for FMD in min-iature swine are likely to apply also to other foreign animal disease pathogens. Education of miniature swine owners and small animal veterinarians about proper food waste feeding and biosecurity practices may help mitigate dis-ease risk in this population of susceptible pet pigs.

a. A copy of the e-mail sent to potential participants is available at: fmd.ucdavis.edu/cadms/pbpcover.html. Accessed Nov 29, 2006.

b. Survey Monkey, SurveyMonkey.com LLC, Portland, Ore. Availa-ble at: www.surveymonkey.com. Accessed Nov 29, 2006.

c. ArcMap, version 9.0, ESRI, Redlands, Calif.d. Google Maps, Google Inc, Mountain View, Calif. Available at:

maps.google.com. Accessed Nov 29, 2006.e. MapQuest MapQuest Inc, Denver, Colo. Available at: mapquest.

com. Accessed Nov 29, 2006.f. Google Earth, Google Inc, Mountain View, Calif. Available at:

earth.google.com. Accessed Nov 29, 2006.g. Ashcraft M, Animal Health Branch, California Department of

Food and Agriculture, Sacramento, Calif: Personal communica-tion, 2006.

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