Knowledge, Attitudes and Practices of Licensed Dog Breeders in Kansas Regarding Canine Brucellosis. By Allison Crow (Melia)

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Knowledge, Attitudes and Practices of Licensed Dog Breeders in Kansas Regarding Canine Brucellosis By Allison Crow (Melia) allicat@vet.ksu.edu

Kansas Department of Health and Environment (KDHE) Health and Environmental Laboratories Environment Health Care Finance Public Health Source: www.kdheks.gov Bureau of Epidemiology and Public Health Informatics (BEPHI) Infectious disease epidemiology and response Disease investigations Investigative reports Statistics

Field Experience Knowledge, Attitudes and Practices Survey Brucellosis Reporting in Humans Brucellosis Reporting in Dogs

BACKGROUND

Canine Brucellosis Infectious reproductive disease of dogs Clinical Signs Males prostatitis, epididymitis, infertility Females abortion, stillbirth, infertility Zoonotic Causes flu-like illness in humans Fever, weakness, night sweats, fatigue, headache, painful joints, unexplained weight loss

Brucella species Gram (-) aerobic coccobacilli Intracellular Smooth or rough colony morphology Bacterial Species Brucella abortus Brucella melitensis Brucella suis Brucella ovis Brucella canis Preferred Host Cattle Sheep and Goats Swine Sheep Dogs

Transmission Direct contact with an infected dog Bacteria can be found in most bodily secretions Highest bacterial load in aborted fetus and vaginal discharge Passed from mother to puppies Transplacental Ingestion of birthing fluids Ingestion of milk Environmental exposure Can survive for months in the environment High humidity, low temperature, no sunlight Source: puppymilk.org/nursing.htm No evidence of human-to-human transmission

Diagnosis in Dogs Serology tests Rapid slide agglutination test (RSAT) Modified RSAT with 2-mercaptoethanol National Veterinary Services Laboratory (NVSL) Confirmatory tests Blood culture PCR Kansas State Veterinary Diagnostic Lab (KSVDL) Photo source: http://www.vet.k-state.edu/depts/dmp/service/

Diagnosis in Humans Human serologic tests use smooth coated antigen Brucella canis has a rough coat False negative Blood culture can also be unreliable Fastidious organism Empiric antibiotic treatment Indirect ELISA??

Treatment Dogs often unrewarding Antibiotic therapy Sterilization Euthanasia No vaccine Humans good prognosis Antibiotic therapy Low mortality

Notification Human Cases Reportable! Kansas Department of Health and Environment Suspect or confirmed cases are to be reported to KDHE within 7 days Local health department KDHE assigns the case to the local jurisdiction Brucellosis Disease Investigation Guidelines Centers for Disease Control and Prevention (CDC) State health departments report cases to CDC

Disease Investigation Guidelines 1. Use current case definition to confirm diagnosis with medical provider 2. Conduct a case investigation to identify potential source of infection 3. Conduct contact investigation to identify additional cases 4. Identify whether the source of infection is a major public health concern 5. Initiate control and prevention measures to prevent spread of disease 6. Complete and report all information requested via the state electronic surveillance system (EpiTrax) 7. Use the disease fact sheet to educate individuals or groups

Notification Dog Cases Reportable! Kansas Department of Agriculture (KDA) Animal Health Division (KDA-AHD) Receives cases from veterinarians or laboratories Disease management KDA-AHD, attending veterinarian and owner collaborate Regulations outlined in Kansas Statutes KSA 47-610 to KSA 47-635

Canine Brucellosis in Humans Centers for Disease Control and Prevention 100+ cases of all Brucella species in the U.S. per year 50 cases total of Brucella canis in the U.S. since 1973 Seroprevalence rates in humans unknown Estimated to account for 1% of all Brucella cases Wide range of estimates from serology surveys 13% in hospital patients in Mexico 0.4% in US military population 0.6% in Florida residents

Canine Brucellosis in Dogs Little data is available on prevalence Estimated 1 8% of U.S. dog population is infected More prevalent in stray dogs and shelter dogs KDA-AHD receives 6 12 cases/year in Kansas

Objectives 1. Knowledge, Attitudes and Practices Survey - Determine licensed dog breeders knowledge, attitudes and practices regarding Brucella canis infection in dogs and humans - Screen licensed dog breeders for a history of symptoms that could suggest human cases of canine brucellosis 2. Brucellosis Reporting in Humans - Assess the human burden of Brucella infection in Kansas 3. Brucellosis Reporting in Dogs - Current case investigation guidelines in place for investigating canine brucellosis cases in breeding facilities

METHODS

KAP Survey 44 multiple choice and free text questions Sent to all 294 licensed breeders in Kansas Physical addresses provided by KDA-AHD One wave of surveys mailed; no follow-up actions Covered various aspects of canine brucellosis Knowledge of disease in dogs and humans Attitudes toward testing dogs for canine brucellosis Personal protective behaviors to reduce transmission History of symptoms of disease in respondents

Licensed Breeders Hobby Sells 3-5 litters a year Animal Breeder Sells 6+ litters a year, primarily for wholesale Retail Breeder Sells 6+ litters a year, primarily at retail Animal Breeder and Distributor

Brucellosis Reporting in Humans Searched for reported Brucella cases in Kansas using the electronic surveillance systems maintained by KDHE Kansas Electronic Disease Surveillance System (KS-EDSS) Used from 1997 2012 EpiTrax databases New reporting system implemented in 2012

Case Definition Case Classification for Brucella Infection Confirmed Clinically compatible illness Definitive laboratory evidence of Brucella infection Probable Suspect Clinical compatible illness with at least one of the following - Epidemiologically linked to a confirmed human or animal brucellosis case - Presumptive laboratory evidence Laboratory results only No clinical information Source: http://wwwn.cdc.gov/nndss/script/casedef.aspx?condyrid=625&datepub=1/1/2010%2012:00:00%20am

Brucellosis Reporting in Dogs Spoke with KDA-AHD about brucellosis reporting Dr. Paul Grosdidier Dr. James Crawford Performed a search for specific laws governing the regulatory authority of KDA-AHD with regard to reportable infectious diseases Kansas Statutes Annotated (KSA) Kansas Pet Animal Act

Statistical Analysis Data grouped into 2x2 contingency tables Fisher s exact two-tailed tests were performed Significance of associations was determined P < 0.05 was considered significant

RESULTS

Response Rate Surveys sent N = 294 Not returned N = 216 Surveys returned N = 78 Not analyzed N = 3 Surveys analyzed N = 75 Response Rate = 25.5%

Breeder Demographics Age: 57.3% below 60; 42.7% above 60 Sex: 17.1% male; 80.5% female Education: 45.1% completed high school only; 54.9% completed some level of higher education Income: 37.8% below $50,000; 30.5% above $50,000; 30.5% prefer not to answer

Breeding Facilities Size of Breeding Facilities Operated by Breeders Median Minimum Maximum Breeding females 15 2 624 Breeding males 6 0 175 Litters produced per year 10 2 250

Knowledge of Disease All breeders N = 75 Have not heard of brucellosis N = 9 Do not know of zoonosis N = 22 Heard of brucellosis N = 66 Know of zoonosis N = 44 88% of breeders have heard of canine brucellosis 66.7% of breeders know that canine brucellosis is zoonotic

Zoonosis vs Education Breeders who know that canine brucellosis is zoonotic, stratified by highest level of education completed Level of Education Knew of Zoonosis Yes No Total College 26 5 31 High School 16 14 30 Total 42 19 61 Fisher s exact test (two tailed): 0.0134 Prevalence ratio: 1.57

Knowledge of Disease Transmission in Dogs In what ways can canine brucellosis be spread from dog to dog? Mode of Transmission Contact with vaginal discharge or products of abortion from an infected bitch Number of Respondents 52 (78.8%) Contact with urine from an infected male 37 (56.1%) Shared food and water bowls 15 (22.7%) Infection passed from infected mother to puppies during pregnancy or whelping 39 (59.1%) Tick bite 4 (6.1%) Sexual contact during natural breeding 59 (89.4%) Use of artificial insemination 26 (39.4%) Not sure 5 (7.6%)

Knowledge of Disease Transmission in Humans How can humans become infected by canine brucellosis? Mode of Transmission Number of Respondents Petting or touching a dog s fur 7 (15.2%) Breathing in the bacteria by nose or mouth 9 (19.6%) Getting licked on the face or mouth by an infected dog Direct contact with abortion material or vaginal discharge from an infected dog 11 (23.9%) 40 (87.0%) Not sure 6 (13.0%)

Knowledge of Disease in Dogs Can dogs that are spayed or neutered get infected with canine brucellosis? Yes No Not sure 37 (56.1%) 11 (16.7%) 18 (27.3%) Is it possible for dogs that have never been bred to have canine brucellosis? Yes No Not sure 51 (77.3%) 7 (10.6%) 7 (13.7%) Can canine brucellosis in dogs be cured? Yes No Not sure 10 (15.2%) 44 (66.7%) 11 (16.7%)

Knowledge of Disease in Humans Can canine brucellosis be spread from person to person? Yes No Not sure 10 (21.7%) 11 (23.9%) 24 (52.2%) Can canine brucellosis in humans be cured? Yes No Not sure 15 (32.6%) 8 (17.4%) 22 (47.8%)

Brucellosis Testing Do you test dogs in your kennel for canine brucellosis? Testing 42% 58% Yes No

Reasons for Testing Dogs When do you test your dogs for brucellosis? Reasons for Testing Number of Respondents Test dogs that have fertility problems 17 (37.0%) Test dogs on a veterinarian s recommendation 12 (26.1%) Test all breeding stock once a year 0 (0.0%) Test dogs prior to each breeding event 2 (4.3%) Test new animals before co-mingling 36 (78.3%) Other 7 (15.2%)

Reasons for Not Testing Dogs What reasons made you decide not to test your dogs? Reason for Not Testing Number of Respondents Did not know about the disease 7 (21.2%) Do not consider my dogs at risk of getting the disease 15 (45.5%) No fertility problems in my kennel 15 (45.5%) Do not want to know if dog is positive 0 (0.0%) Testing takes too much time and effort 0 (0.0%) Testing is too expensive 5 (15.2%) Other 9 (27.3%)

Testing vs History of Infertility Breeders who test dogs, stratified by history of infertility History of Infertility Perform testing Yes No Total Yes 18 6 24 No 24 24 48 Total 42 30 72 Fisher s exact test (two tailed): 0.0478 Prevalence Ratio: 1.50

Number of Tests Performed Number of tests performed and number of dogs diagnosed with brucellosis Past 5 years Total tests Test (+) dogs Diagnosed dogs 2086 63 63 Past 12 Months Total Tests Test (+) dogs Diagnosed dogs 697 18 18 A total of seven breeders reported having positive dogs

Sources of Breeding Dogs Source Number of Respondents Buy dogs from other breeders 52 (69.3%) Buy dogs from auction events 16 (21.3%) Keep some of own puppies to breed 72 (96.0%) Buy semen and use AI 5 (6.7%) Other 4 (5.3%)

Auctions vs Positive Dogs Breeders who buy dogs from auctions, stratified by breeders with brucellosis-positive dogs Purchase dogs from auctions Positive Dog(s) Yes No Total Yes 5 11 16 No 2 57 59 Total 7 68 75 Fisher s Exact test (two tailed): 0.0040 Prevalence Ratio: 9.20

Practicing Personal Protection Do you wear gloves when performing the following activities? Activity Do Wear Gloves Routine cleaning of cages/runs 35 (46.7%) Assisting in whelping puppies 37 (49.3%) Cleaning the area after whelping 35 (46.7%)

Symptoms of Human Disease Within two months of any stillbirth or abortion in your kennel, did you notice any of the following symptoms in yourself? Fever Night sweats Painful joints Weight loss Headache Fatigue Weakness Arthritis/back pain Response We have never had a stillbirth or abortion in the kennel Number of Respondents 22 (29.7%) I had none of these symptoms 46 (62.2%) Fatigue 1 (1.4%) No response 5 (6.8%)

Brucellosis Reporting in Humans Brucellosis cases in Kansas, 1997-2012 Case Classification Number of cases Confirmed 11 Probable 16 Suspect 28 Total = 55 cases Only five confirmed cases listed a specific Brucella species Four cases reported B. melitensis as the causative agent One case reported B. abortus as the causative agent

Brucellosis Reporting in Dogs KDA-AHD does not currently have a written protocol guiding case investigation upon report of a brucellosis-positive dog in a breeding facility Regulatory actions for all reportable infectious diseases are outlined in the Kansas Statutes Annotated (KSA) and Kansas Administrative Regulations (KAR)

KAR 9-27-1 Includes all species of brucellosis in the list of diseases that shall be designated as reportable infectious or contagious animal diseases and shall be reported in accordance with KSA 47-622.

KSA 47-622 It is the duty of any person who discovers the existence of any such contagious or infectious disease among the domestic animals of any person to immediately report this information to the animal health commissioner.

KSA 47-610 [The] state animal health commissioner is directed to protect the health of domestic animals of the state from all contagious and infectious diseases and for this purpose is hereby authorized and empowered to establish, maintain and enforce such quarantine, sanitary and other regulations as necessary.

KSA 47-634 The state animal health commissioner can impose mandatory disinfection of the premises where a disease animal or animals have been housed.

KSA 47-614 When in the opinion of the commissioner it shall be necessary to prevent the spread of any contagious or infectious diseases among the domestic animals of this state, to destroy animals affected with or which have been exposed to any such disease, or which are unconfined in violation of any quarantine order, he shall determine what animals shall be killed and cause the same to be killed and the carcasses disposed of as in his judgment will best protect the health of the domestic animals of the locality.

CONCLUSIONS AND DISCUSSION

Conclusions Licensed dog breeders in Kansas are more knowledgeable about canine brucellosis in dogs than in humans While breeders know that canine brucellosis is zoonotic, this knowledge does not translate into the performance of appropriate protective behaviors such as wearing gloves when in contact with potentially infected dogs Attitudes toward testing are more favorable regarding newly purchased dogs than currently owned dogs No breeders reporting symptoms of disease

Limitations Small study size Response rate = 25.5% Comparison of respondents vs non-respondents Based on region of KS where breeder was located Not statistically different Power of study Limited ability to find significant associations Limited ability to find a breeder with symptoms of disease

Limitations Recall bias Many responses based on memory of past events Symptoms of disease in humans are non-specific Events of interest (ex abortion) may have happened years previously

Limitations Each of the seven respondents reporting positive dogs in their facility wrote the same number for dogs that tested positive and dogs that were diagnosed Respondents indicated confusion in the distinction between the two terms Questions were intended to differentiate dogs that tested positive on a screening test (not 100% specific) and those that were ultimately diagnosed These data should not be used alone to assess disease burden in this population

Discussion Knowledge of disease Breeders know much more about canine brucellosis in dogs than in humans Knowledge of the zoonotic potential does not translate into personal protective practices such as wearing gloves Low perceived risk of infection

Discussion Attitudes toward testing Breeders commonly test newly purchased dogs before introducing them into the kennel (81%) Breeders are much less likely to test dogs that are already in the facility, even if they develop fertility problems (41%) Reluctance to test could be due to regulatory implications of having a positive dog

Discussion Reasons for not finding any human cases Small sample size with a rare disease Symptoms are non-specific and may be mild Under-reporting

Discussion Why estimates of human disease burden of canine brucellosis may be falsely low Non-specific clinical signs False negative serologic tests Standard brucellosis tests do not detect Brucella canis Doctors may not consider B. canis as a differential CDC does not require that the etiologic species of Brucella be included in case reports

Recommendations KDHE and KDA-AHD Develop a joint protocol to follow-up on reported cases of canine brucellosis that may have resulted in human exposure Create a fact sheet to provide to breeders Incubation period and length of symptom watch What symptoms may develop What to do if you develop symptoms Include the specific causative agent of Brucella in any case reported entered into EpiTrax

Recommendations Further study Serosurveillance More accurate assessment of prior exposure Determine risk factors for those with seroconversion Education Outreach to breeders to increase knowledge Encourage proper protective behaviors

Acknowledgements We would like to thank: KDA-AHD, Dr. Paul Grosdidier and Dr. James Crawford for providing contact information Breeders for their participation in the survey KDHE s Environmental Public Health Tracking Program for financial support Ms. Janet Neff and Ms. Shelley Bearman for assisting in printing and mailing the surveys

References Center for Food Security and Public Health. Brucellosis. Powerpoint presentation. Created 2008. Accessed 7/9/2012. Purcell, Bret K., David L. Hoover, and Arthur M. Friedlander. Chapter 9 Brucellosis. Medical Aspects of Biological Warfare. Retrieved 7/9/2012 from http://www.bordeninstitute.army.mil/published_volumes/biological_warfare/bw-ch09.pdf The Center for Food Security and Public Health. Canine Brucellosis: Brucella canis. Retrieved 6/14/2012 from http://www.ivis.org/advances/disease_factsheets/brucellosis_canis.pdf. Kazmierczak, Jim. Public Health Implication of Brucella canis Infections in Humans. March 2012. Retrieved 5/16/2012 from http://www.nasphv.org/documents/brucellacanisinhumans.pdf. Sayan, Murat, Judy Stack, et al. A Serological Diagnostic Survey for Brucella canis Infection in Turkish Patients with Brucellosis-Like Symptoms. Journal of Infectious Disease, 64, 516-519, 2011. Lucero, Nidia E., Gabriela I. Escobar, Sandra M. Ayala, and Nestor Jacob. Diagnosis of human brucellosis caused by Brucella canis. Journal of Medical Microbiology (2005), 54, 457-461. Nagaraja, T.G. Brucella. Class notes from personal collection. Retrieved 7/9/2012. Young, Edward J. An Overview of Human Brucellosis. Clinical Infectious Diseases, Vol. 21, No. 2 (Aug., 1995). Retrieved 8/26/2012 from http://www.jstor.org/stable/4458778. Hollett, R. Bruce. Canine brucellosis: Outbreaks and compliance. Theriogenology 66 (2006) 575-587. Almes, Kelli. Personal communication. December 19, 2012

References Georgia Department of Agriculture. Canine Brucellosis (Brucella canis). Retrieved 7/9/2012 from http://www.agr.georgia.gov/data/sites/1/media/ag_animalindustry/animal_health/files/caninebr ucellosis.pdf. Centers for Disease Control and Prevention. Laboratory-Acquired Brucellosis Indiana and Minnesota, 2006. Morbidity and Mortality Weekly Report. January 18, 2008 / 57(02); 39-42. Lucero, N.E., G.I. Escobar, S.M. Ayala, and g. Lopez. Sensitivity and specificity of an indirect enzyme-linked immunoassay for the diagnosis of Brucella canis infection in dogs. Journal of Medicine and Microbiology, Vol. 51 (2002), 656-660. Kansas Pet Animal Act [PDF file]. Retrieved 2/17/2013 from http://www.kansas.gov/kahd/pdf/laws/kpaa.pdf. Animal Health Statutes [PDF file]. Retrieved 2/17/2012 from http://www.ksda.gov/includes/statute_regulations/mainportal/animinal_health.pdf Garrison, Ingrid. B. canis Survey. Survey. 16 May 2012. Kansas Department of Health and Environment. Brucellosis Investigation Guideline. Version 07/2012. Retrieved 7/9/2012 from http://www.kdheks.gov/epi/investigation_guidelines/brucellosis_investigation_guideline.pdf. Survey Random Sample Calculator. Accessed 2/20/2013. http://www.custominsight.com/articles/random-sample-calculator.asp Moser, Karin. The Green, the Blue and the Toxic: Knowledge, Attitudes and Practices of Physicians and Veterinarians Regarding Harmful Algal Blooms. K-State Research Exchange (K-REx). Accessed 1 September 2012 from http://krex.k-state.edu/dspace/handle/2097/14204. Centers for Disease Control and Prevention. Brucellosis (Brucella spp.). National Notifiable Diseases Surveillance System. Retrieved 8/25/2012 from http://www.cdc.gov/osels/ph_surveillance/nndss/casedef/brucellosis_current.htm.

Questions? allicat@vet.ksu.edu