Importation of dogs into the United States: risks from rabies and other zoonotic diseases

The importation of dogs into the United States poses a risk for the introduction of rabies and other zoonotic diseases. Federal regulations (42 CFR 71.51) currently require proof of valid rabies vaccination for imported dogs, but allow the importation of some unvaccinated dogs, including dogs less than 3 months of age, provided certain requirements for confinement are met until the dog is vaccinated. Although there are no accurate surveillance data on the number of dogs imported each year, it is estimated based on extrapolated data that over 287,000 dogs were imported into the United States during 2006. Of these, approximately 25% were either too young to be vaccinated or lacked proof of valid rabies vaccination. Import trends suggest that an increasing number of unvaccinated puppies are being imported into the United States, many through commercial resale or rescue operations. Since 2004, foreign canine rabies virus variants have been documented in at least two imported puppies. Federal regulations are currently being reviewed by the Centers for Disease Control and Prevention to determine if they can be updated to address current import trends and disease risks, such as requiring a health screen and valid rabies vaccinations for all dogs prior to entry.     

State and Local Perspective on Implementation of the Centers for Disease Control and Prevention Dog Confinement Agreement

The Centers for Disease Control and Prevention (CDC) works in conjunction with state, territorial, local and tribal agencies (STLTAs) to prevent the transmission of infectious agents. Issuance of confinement agreements using CDC Form 75.37 ‘Notice to Owners and Importers of Dogs’ to importers of dogs that are not vaccinated or incompletely vaccinated against rabies is part of the agency's regulatory programme to prevent the entry of dogs infected with rabies. Although this is a regulatory programme that depends heavily on partnerships between CDC and STLTAs, CDC had never formally evaluated the acceptability of the confinement agreement process with these partners. Thus, a short survey of nine STLTAs was conducted to evaluate whether these partners have enough personnel and resources to implement the regulation and their general opinions of the confinement agreement process. The results illustrate that CDC partners are dissatisfied to some extent with the process, and there are multiple issues limiting their success in enforcing the regulation.     

Canine Rabies in Australia: A Review of Preparedness and Research Needs

Australia is unique as a populated continent in that canine rabies is exotic, with only one likely incursion in 1867. This is despite the presence of a widespread free‐ranging dog population, which includes the naturalized dingo, feral domestic dogs and dingo‐dog cross‐breeds. To Australia's immediate north, rabies has recently spread within the Indonesian archipelago, with outbreaks occurring in historically free islands to the east including Bali, Flores, Ambon and the Tanimbar Islands. Australia depends on strict quarantine protocols to prevent importation of a rabid animal, but the risk of illegal animal movements by fishing and recreational vessels circumventing quarantine remains. Predicting where rabies will enter Australia is important, but understanding dog population dynamics and interactions, including contact rates in and around human populations, is essential for rabies preparedness. The interactions among and between Australia's large populations of wild, free‐roaming and restrained domestic dogs require quantification for rabies incursions to be detected and controlled. The imminent risk of rabies breaching Australian borders makes the development of disease spread models that will assist in the deployment of cost‐effective surveillance, improve preventive strategies and guide disease management protocols vitally important. Here, we critically review Australia's preparedness for rabies, discuss prevailing assumptions and models, identify knowledge deficits in free‐roaming dog ecology relating to rabies maintenance and speculate on the likely consequences of endemic rabies for Australia.     

Factors Associated with Dog Rabies Vaccination in Bhol,Philippines: Results of a Cross‐Sectional Cluster Survey Conducted Following the Island‐Wide Rabies Elimination Campaign

The Philippines has a long history of rabies control efforts in their dog populations; however, long‐term success of such programmes and the goal of rabies elimination have not yet been realized. The Bohol Rabies Prevention and Elimination Program was developed as an innovative approach to canine rabies control in 2007. The objective of this study was to assess canine rabies vaccination coverage in the owned‐dog population in Bohol and to describe factors associated with rabies vaccination 2 years after implementation of the programme. We utilized a cross‐sectional cluster survey based on the World Health Organization’s Expanded Programme on Immunization coverage survey technique. We sampled 460 households and collected data on 539 dogs residing within these households. Seventy‐seven per cent of surveyed households reported owning at least one dog. The human‐to‐dog ratio was approximately 4 : 1, and the mean number of dogs owned per household was 1.6. Based on this ratio, we calculated an owned‐dog population of almost 300 000. Overall, 71% of dogs were reported as having been vaccinated for rabies at some time in their lives; however, only 64% of dogs were reported as having been recently vaccinated. Dogs in our study were young (median age = 24 months). The odds of vaccination increased with increasing age. Dogs aged 12–23 months had 4.6 times the odds of vaccination compared to dogs aged 3–11 months (95% CI 1.8–12.0; P = 0.002). Confinement of the dog both day and night was also associated with increased odds of vaccination (OR = 2.1; 95% CI 0.9–4.9; P = 0.07), and this result approached statistical significance. While the programme is on track to meet its goal of 80% vaccination coverage, educational efforts should focus on the need to confine dogs and vaccinate young dogs.     

Is That a Rodent in Your Luggage? A Mixed Method Approach to Describe Bushmeat Importation into the United States

Bushmeat, defined as meat derived from wild animals, is a potential source of zoonotic pathogens. Bushmeat from restricted animals is illegal to import into the United States under US federal regulations. We reviewed US Centers for Disease Control and Prevention (CDC) port of entry surveillance records from September 2005 through December 2010 and conducted focus group studies to describe trends in and reasons for bushmeat importation into the United States. In total, 543 confiscated bushmeat items were recorded. Half of the confiscated bushmeat items identified were rodents. Africa was the most frequent continent of origin. Seasonality was evident, with bushmeat confiscations peaking in late spring to early summer. Four times more bushmeat was confiscated during an enhanced surveillance period in June 2010 compared with the same period in previous years, suggesting that routine surveillance underestimated the amount of bushmeat detected at US Ports of Entry. Focus groups held in three major US cities revealed that bushmeat importation is a multifaceted issue. Longstanding cultural practices of hunting and eating bushmeat make it difficult for consumers to acknowledge potential health and ecologic risks. Also, US merchants selling African goods, including bushmeat, in their stores have caused confusion among importers as to whether importation is truly illegal. Enhancing routine surveillance for bushmeat and consistent enforcement of penalties at all ports of entry, along with health education aimed at bushmeat importers, might be useful to deter illegal importation.     

Comparison of behavioral characteristics of dogs in the United States and Japan

This study examined the difference in dog owning between Japan and the United States, and the effect of these differences on dogs’ behavioral characteristics. Behavioral evaluations of privately-owned dogs were obtained by using online questionnaire. We compared background and demographic information from the two countries and analyzed the effects of these differences on behavioral characteristics in dogs. The results indicated that there was a bias in the dog breeds kept in Japan compared to the United States and that Japanese dogs’ body weight was lower than the US dogs. The main source of dog acquisition was pet stores in Japan and breeders and/or shelters in the United States. Multiple linear regression analysis found that Japanese dogs showed more aggression to household members and higher energy, restlessness and fear of non-social stimuli than US dogs, while US dogs showed more fear of unfamiliar persons, separation-related behavior and excitability. US dogs also showed higher levels of trainability and attachment to owners. The lower dog’s body weight was, the higher the behavioral scores except for trainability were. When dogs that were obtained under 3 months of age were analyzed, the younger the dogs were when their owners obtained them, the higher the scores on some behavioral problem factors were. The higher rates of problem behaviors among Japanese dogs compared with US dogs suggest that the preference for small breed dogs and poor early development environment influenced the behavioral characteristics of dogs.     

Canine ecology and socioeconomic factors associated with dogs unvaccinated against rabies in a Mexican city across the US-Mexico border

A cross-sectional study was conducted to identify ecologic and socioeconomic factors associated with dogs unvaccinated against rabies in Mexicali, the capital city of Baja California, Mexico (located across the US-Mexico border). A total of 1100 households were selected by random sampling from a list of all 180,000 households. A questionnaire was filled in during a personal interview with the household head or another adult person to gather information of epidemiological interest (such as canine ecology, social and economic factors that might influence owners' decision to allow their dog to be vaccinated). There were 910 dogs identified. The human-to-dog ratio was 4.3:1. The male-to-female dog ratio was 1.5:1. Out of 791 dogs > or = 3 months old, 577 (73%) were classified as vaccinated against rabies. Most dogs (95%) were not spayed. Neighborhood dogs had 25 times higher risk of nonvaccination compared to dogs owned by a family. Dogs 3-11 months old had three times higher risk of nonvaccination compared to dogs > or = 1 year old. Dogs that were obtained as a gift, born at home or found had two times higher risk of nonvaccination compared to dogs that were reportedly purchased. Crossbred dogs had 1.5 times higher risk of nonvaccination compared to purebred dogs. The canine-ecology structure is similar to that in regions were rabies is endemic.     

Development of non‐governmental organisation‐academic partnership to tackle rabies in Africa and Asia

Rabies kills approximately 60,000 people each year, mainly in sub‐Saharan Africa and Asia, of which 40% of victims are less than 15 years old. Once clinical signs develop, the disease is almost invariably fatal. Globally, rabies has been estimated to cause 3?7 million disability‐adjusted life years and $8?6B in economic losses annually. The vast majority of human rabies cases are caused by bites from rabies‐infected dogs. Despite this loss of human life and resultant economic and societal costs, rabies can be prevented in both humans and dogs by vaccination. This has been demonstrated in many countries, notably in Central and South America, where large‐scale, high coverage mass dog vaccination programmes have dramatically reduced the incidence of rabies. Even in parts of Africa and Asia, projects have shown that rabies can be eliminated locally. Nevertheless, rabies remains an important cause of mortality in many sub‐Saharan and Asian countries. The reasons why some countries have been able to effectively eliminate rabies whereas others have not are complex and often impossible to definitively identify; commonly cited explanations include political, economic, logistical and societal barriers.     

Factors associated with rabies vaccination of dog shelter staff in the United States

US animal shelters house and care for dogs with unknown medical histories. Such unknown medical backgrounds pose concern for zoonotic transmission of diseases to the shelter staff. One important zoonotic exposure is to rabies virus which is almost always fatal after the onset of symptoms. The objective of this study was to identify the characteristics of dog shelters associated with the probability that the shelter had a policy to vaccinate shelter personnel against rabies. Five states with an established shelter registry were selected from each geographic region of the United States. A list of shelters within those states was developed from the registry list, through Internet searches and comparisons with other known lists. At least two forms of direct communication were used to ensure that humane organizations met the study definition of a dog shelter. In total, 342 of 461 (73%) shelters that met the study definition were visited by a team of students. Forty‐two of 332 (13%) shelters responding to the question required staff to be vaccinated against rabies. Logistic regression was utilized to test shelter characteristics for association with the probability that they have a rabies vaccination policy for shelter staff. Municipally funded shelters were more likely to vaccinate staff for rabies than shelters funded privately (OR = 3.0, 95% CI = 1.40–6.39). These results demonstrate that shelter funding source may influence rabies control programmes in shelters.     

Expert Opinion to Identify High‐Risk Entry Routes of Canine Rabies into Papua New Guinea

The proximity of Papua New Guinea (PNG) to canine rabies‐endemic countries in South‐East Asia presents a risk of incursion of this disease into PNG and the rest of the Oceanic region. The objective of this study was to identify the highest risk routes for entry of dogs – associated with movement of people – into PNG from canine rabies‐endemic countries. A structured, in‐country expert‐elicitation workshop was used, and 20 entry routes were identified. The highest risk routes were three land routes from Papua, Indonesia (hunters, traditional border crossers and unregulated, unchecked ‘shopper‐crossers’) and two sea routes (fishing and logging). These results will be used to direct more detailed risk assessments to develop surveillance strategies and incursion response plans.     

Free‐Roaming Dogs in Nepal: Demographics,Health and Public Knowledge,Attitudes and Practices

In Nepal, most dogs are free to roam and may transmit diseases to humans and animals. These dogs often suffer from malnutrition and lack basic health care. Minimal information is available about their demographics and about public attitudes concerning dogs and diseases. We carried out a study in Chitwan District (central Nepal), to collect baseline data on free‐roaming owned dog demographics, assess knowledge, attitudes and practices of dog owners concerning dogs and rabies, evaluate rabies vaccination coverage and anthelmintic treatment of dogs, measure dogs' response to rabies vaccination and assess dog health through body condition scores and parasites. We conducted household interviews with owners of free‐roaming female dogs (n = 60) and administered dogs with rabies vaccination and anthelmintics. Dog owners regularly fed free‐roaming dogs but provided minimal health care; 42% of respondents did not claim ownership of the dog for which they provided care. We collected skin, faecal and blood samples for parasite identification and for measuring rabies virus‐specific antibodies. Ninety‐two per cent of dog owners were aware of the routes of rabies virus transmission, but only 35% described the correct post‐exposure prophylaxis (PEP) following a dog bite. Twenty‐seven per cent of the dogs had measurable rabies virus‐specific antibody titres and 14% had received anthelmintics in the previous year. Following rabies vaccination, 97% of dogs maintained an adequate antibody titre for ≥6 months. Most dogs appeared healthy, although haemoprotozoans, endoparasites and ectoparasites were identified in 12%, 73% and 40% of the dogs, respectively. Poor skin condition and parasite load were associated. Seventy‐four per cent of the females had litters in 1 year (mean litter size = 4.5). Births occurred between September and February; we estimated 60% mortality in puppies. We concluded that vaccination coverage, PEP awareness and anthelmintic treatment should be emphasized in educational programmes focussed on animal welfare, veterinary and public health.     

A Comparative Study of the RAPINA and the Virus‐Neutralizing Test (RFFIT) for the Estimation of Antirabies‐Neutralizing Antibody Levels in Dog Samples

The mass vaccination of dogs against rabies is a highly rational strategy for interrupting the natural transmission of urban rabies. According to the World Organization for Animal Health (OIE) and the World Health Organization (WHO), the immunization of at least 70% of the total dog population minimizes the risk of endemic rabies. Knowledge of the virus‐neutralizing antibody (VNA) level against the rabies virus (RABV) is required to evaluate protective immunity and vaccine coverage of dogs in the field. The rapid focus fluorescent inhibition test (RFFIT) and the fluorescent antibody virus neutralization (FAVN) test are recommended by OIE and WHO to determine the VNA levels in serum. However, these tests are cell culture based and require the use of live viruses and specialized equipment. The rapid neutralizing antibody test (RAPINA) is a novel, immunochromatographic test that uses inactivated virus to estimate the VNA level qualitatively. It is a simple, rapid and inexpensive, although indirect, assay for the detection of VNA levels. The RAPINA has shown good positive and negative predictive values and a high concordance with the RFFIT results. In this study, we compared the performance of the two tests for evaluating the vaccination status of dogs in the Philippines, Thailand and Japan. A total of 1135 dog sera were analysed by the RAPINA and compared to the VNA levels determined by the RFFIT. The overall positive and negative predictive values of the RAPINA were 96.2–99.3% and 84.5–94.8%, respectively, with a concordance (kappa) of 0.946–0.97 among the three countries. The RAPINA results were highly homologous and reproducible among different laboratories. These results suggest that this test is appropriate to survey vaccination coverage in countries with limited resources.     

镇江市2008年兽用狂犬病疫苗免疫效果观察

为评价镇江市家犬兽用狂犬病疫苗的免疫效果,探讨影响免疫效果的因素,采集镇江市不同地区免疫犬和非免疫犬只的血清样本,ELISA法测定其抗体产生情况。结果表明,镇江市总的免疫犬只抗体阳性率为34．53％（67／194）;不同地区犬只抗体阳性率差异显著（χ2 =23．743,P=O．000）;犬只的免疫3剂次及以上与3剂次以...     

Rabies surveillance in the United States during 2006

During 2006, 49 states and Puerto Rico reported 6,940 cases of rabies in animals and 3 cases in humans to the CDC, representing an 8.2% increase from the 6,417 cases in animals and 1 case in a human reported in 2005. Approximately 92% of the cases were in wildlife, and 8% were in domestic animals. Relative contributions by the major animal groups were as follows: 2,615 raccoons (37.7%), 1,692 bats (24.4%), 1,494 skunks (21.5%), 427 foxes (6.2%), 318 cats (4.6%), 82 cattle (1.2%), and 79 dogs (1.1%). Compared with numbers of reported cases in 2005, cases in 2006 increased among all groups except cattle. Increases in numbers of rabid raccoons during 2006 were reported by 11 of the 20 eastern states where raccoon rabies was enzootic, and reported cases increased by 3.2% overall, compared with 2005. On a national level, the number of rabies cases in skunks during 2006 increased by 6.1% from the number reported in 2005. Once again, Texas reported the greatest number (n = 351) of rabid skunks and the greatest overall state total of animal rabies cases (889). No cases of rabies associated with the dog/coyote rabies virus variant were reported. The last identified case of this canine rabies virus variant was identified in March 2004, along the US/Mexico border. With 2006 marking the second year of no apparent transmission of the dog/coyote variant, these findings from surveillance data support the contention that the canine rabies virus variant is no longer in circulation in the United States. Total number of cases of rabies reported nationally in foxes increased 13.6%, compared with 2005. Increases in the number of reported rabid foxes were attributable to greater numbers of foxes reported with the Arctic fox rabies virus variant in Alaska, the Texas gray fox rabies virus variant in Texas, and the raccoon rabies virus variant in Virginia. The 1,692 cases of rabies reported in bats represented a 14.5% increase, compared with numbers reported in 2005, making bats the second most reported rabid animal behind raccoons. Cases of rabies in cats, dogs, horses and mules, and sheep and goats increased 18.2%, 3.9%, 12.8%, and 22.2%, respectively, whereas cases reported in cattle decreased 11.8%. In Puerto Rico, reported cases of rabies in mongooses increased 9.2%, and rabies in domestic animals, presumably attributable to spillover infection from mongooses, increased 20%. Three cases of human rabies were reported from Texas, Indiana, and California during 2006. The cases in Indiana and Texas were attributed to bat rabies virus variants, whereas the case in California was attributed to an exposure to a dog in the Philippines.     

Epidemiologic factors, clinical findings, and vaccination status of rabies in cats and dogs in the United States in 1988. National Study Group on Rabies

Despite the availability of rabies vaccination through private veterinarians and government-sponsored rabies control programs, rabies was reported in an average of 338 cats and dogs per year from 1980 through 1987 in the United States. Information was collected on 90% of the 183 cats and 97% of the 119 dogs that were reported to have rabies in the continental United States in 1988. The median age of rabid cats and dogs was 1 year, and 81% were from rural areas. Compared with rabid cats, rabid dogs were more likely to have been male (66 vs 42%, odds ratio = 2.6), to have been kept as pets (84 vs 43%, odds ratio = 6.8), and to have had reported contact with wildlife before onset of illness (38 vs 14%, odds ratio = 3.8). Rabid cats accounted for a greater proportion of human rabies postexposure prophylaxis, bites to people, and exposures to other animals than did rabid dogs. Although the clinical signs of rabies varied, rabid cats were more likely than dogs to have had aggressive behavior (55 vs 31%, odds ratio = 2.8). In contrast, rabid dogs were more likely than cats to have had an illness consistent with a paralytic process. The median period between onset of illness and death was 3 days (range, less than 1 to 10) in rabid cats and dogs that were allowed to die of rabies. Vaccine failures were documented in 3 (1%) rabid animals (2 cats and 1 dog). All animals had received only a single dose of vaccine in their lifetime and were vaccinated when they were between 3 and 6 months old.     

Rocky Mountain spotted fever

Rocky Mountain spotted fever is an endemic tickborne disease found throughout the United States and other regions of the world. Exposure may result in a spectrum of disease from subclinical infection to severe or fatal multiorgan collapse. The disease is maintained in nature in Ixodid tick vectors and their hosts. The most important ticks in the United States are Dermacentor variabilis and Dermacentor andersoni. Small mammals are the natural reservoirs in the wild. Dogs become infected when a tick harboring Rickettsia rickettsii feeds on the dog. Dogs do not develop sufficient rickettsemia to act as a reservoir in the transmission of Rickettsia rickettsii. Thus, although dogs act as sentinels to the presence of the disease, they cannot directly transmit infection. Signs in early stages of disease often are nonspecific. The most characteristic laboratory abnormality is thrombocytopenia, but serologic testing is necessary for confirmation of infection. Tetracycline and chloramphenicol are effective antibiotics to treat infection. Treatment should continue for 14 to 21 days to allow host immune defenses to develop and eradicate the organism. Prevention requires avoidance of tick-infested areas and rapid removal of ticks should exposure occur.     

Impact of Rabies Vaccination History on Attainment of an Adequate Antibody Titre Among Dogs Tested for International Travel Certification,Israel – 2010–2014

Rabies is endemic in wildlife or domestic carnivore populations globally. Infection of domestic dogs is of particular concern in many areas. In regions where domestic animals are at risk of exposure to rabies virus, dogs should be routinely vaccinated against rabies to protect both pet and human populations. Many countries require demonstration of an adequate level of serum rabies neutralizing antibodies to permit entry of dogs during international travel. We analysed rabies titres of dogs seeking travel certification in Israel to assess demographic and vaccine history factors associated with antibody titres below the acceptable threshold for travel certification. Having received only one previous rabies vaccination and a longer duration since the most recent vaccination was received were primary risk factors for not achieving an adequate rabies virus neutralizing antibody titre for travel certification. These risk factors had stronger effects in younger animals, but were consistent for dogs of all ages. In particular, these findings reiterate the importance of administering at least two rabies vaccinations (the primo vaccination and subsequent booster) to ensure population‐level protection against rabies in dogs globally.     

Public health response to an imported case of canine melioidosis

Melioidosis in humans presents variably as fulminant sepsis, pneumonia, skin infection and solid organ abscesses. It is caused by Burkholderia pseudomallei, which in the United States is classified as a select agent, with “potential to pose a severe threat to both human and animal health, to plant health or to animal and plant products” (Federal Select Agent Program, http://www.selectagents.gov/ , accessed 22 September 2016). Burkholderia pseudomallei is found in soil and surface water in the tropics, especially South‐East Asia and northern Australia, where melioidosis is endemic. Human cases are rare in the United States and are usually associated with travel to endemic areas. Burkholderia pseudomallei can also infect animals. We describe a multijurisdictional public health response to a case of subclinical urinary B. pseudomallei infection in a dog that had been adopted into upstate New York from a shelter in Thailand. Investigation disclosed three human contacts with single, low‐risk exposures to the dog's urine at his residence, and 16 human contacts with possible exposure to his urine or culture isolates at a veterinary hospital. Contacts were offered various combinations of symptom/fever monitoring, baseline and repeat B. pseudomallei serologic testing, and antibiotic post‐exposure prophylaxis, depending on the nature of their exposure and their personal medical histories. The dog's owner accepted recommendations from public health authorities and veterinary clinicians for humane euthanasia. A number of animal rescue organizations actively facilitate adoptions into the United States of shelter dogs from South‐East Asia. This may result in importation of B. pseudomallei into almost any community, with implications for human and animal health.     

Exploring animal rabies endemicity to inform control programmes in Punjab,India

Previous studies estimate that one‐third of the annual global burden of rabies (~20,000 cases) occurs in India. Elimination of canine rabies is essential to reduce this burden. Surveillance of animal cases can assess both the risk to humans and the efficacy of control strategies. The objective of this study was to describe the spatial and temporal occurrence of reported confirmed cases of rabies in animals in Punjab, India, from 2004 to 2014. We analysed passive surveillance data on 556 samples submitted from 2004 to 2014 to GADVASU, Ludhiana, Punjab, India. Regression and time series analyses were conducted to understand seasonal and long‐term variation of cases and identify cross‐correlation of monthly cases between species. Spatio‐temporal analyses assessed spatial autocorrelation of date of reporting, mean geographic centres of disease occurrence and clustering of cases using Kulldorff's space‐time permutation statistic. The annual number of submissions and proportion of confirmed cases were consistent throughout 2004–2014. Most submissions (320; 57.6%) were confirmed rabies cases, including dogs (40.6%), buffalo (29.7%) and cattle (23.1%). Regression analysis of monthly cases in dogs showed seasonal variation with significant increases in cases in March and August. Monthly case numbers in buffalo decreased over time. Long‐term temporal trend was not detected in dog and cattle cases. Time‐series models identified significant cross‐correlation between dog and buffalo cases, suggesting that buffalo cases were spillover events from dogs. Significant spatio‐temporal variation or clusters of cases were not detected. These results indicate that rabies cases in animals—and therefore, the potential for exposure to humans—were temporally and spatially stable during 2004–2014 in Punjab, India. The endemic nature of rabies transmission in this region demands a coordinated, sustained control programme. This study provides baseline information for assessing the efficacy of rabies control measures and developing seasonally targeted dog vaccination and rabies awareness strategies.