Brucellosis, caused by the bacterium Brucella canis, is a gram-negative bacterium. It is a infectious zoonotic disease (which means it can spread from animal to human), especially for those who are higher risk groups dog breeders, kennel, veterinary and laboratory staff and owners of infected dogs, especially those which are breeding or birthing. Brucella canis is the primary focus of this article because of the need to support the veterinary profession, the public and dog rescue organisations in our attempts to manage, test and recognise the disease in small animal practice.
Brucella Species
Brucellosis is of global significance due to its adverse impact on public health, economics, and trade. Despite being one of the most prevalent zoonoses worldwide, attention given to global brucellosis control and prevention is often inadequate. Brucella species of relevance include those infecting dogs (Brucella canis), swine (Brucella suis), and cattle and domestic bison (Brucella abortus).
In the UK in 2021 Public Health England released a Human Animal Infections and Risk Surveillance HAIRS risk statement that noted since summer 2020 there has been an unexpectedly high number of reports of Brucella canis infection in dogs, mostly directly imported into the UK from Eastern Europe. At that time in the UK there had been no transmission to humans via dogs - this is now sadly not the case. Within a year of the statement the first case of a person being infected with Brucella canis was reported, they had been exposed to the aborted material from a pregnant imported dog. In the UK’s first confirmed dog-to-human transmission of Brucella canis, the woman fostering the dog was hospitalised after coming into close contact. The foster animal and four pet dogs who were exposed to the disease, three of whom also tested positive, all had to be euthanised.
The 2023 HAIRS report noted:
Historically, Brucella canis (B. canis) has not been regarded as endemic in the UK. Since summer 2020, there has been an increase in the number of reports of B. canis infection in dogs, the majority of which have been in dogs directly imported into the UK from Eastern Europe. B. canis is a recognised zoonotic pathogen, but human cases are rarely reported globally
Brucella canis is a reportable disease and was one that the APHA and Defra highlighted when they suspended commercial imports of dogs from Ukraine and neighbouring countries in April. To report Brucella canis in England and Wales, you should contact your local APHA VIC.
The HAIRS statement believed that imported dogs from Brucella canis endemic countries present an ongoing animal and public health risk to the UK.
Foreign Imports are increasing
The UK saw a 50% increase in dogs being imported for rescue during 2020 during the Covid 19 lockdowns - with imports from Romania leaping by nearly 70% as the demand for puppies soared.
In 2020 alone nearly 30 thousand dogs were imported from Romania, over 50% increase from 2019 and NOT taking into account the astonishing number of illegal imports. The number of dogs imported from the EU increased during the lockdowns by 52% - it is important to note that these are only the official figures and don’t take into account illegally imported animals.
More than 66,000 dogs were imported into the UK in 2020 according to Animal and Plant Health Agency figures. However, evidence shows a worrying rise in low-welfare imports and smuggling activity, with border authorities seeing around a 260% increase in the number of young puppies being intercepted for not meeting the UK’s pet import rules.
RSPCA David Bowles, head of public affairs has said that:
"Our frontline investigations into unscrupulous breeders and sellers have uncovered organised criminal gangs who import puppies from overseas - often from Ireland and Eastern European countries such as Romania - to sell on to unsuspecting buyers here in the UK. These latest statistics from Defra just goes to show the scale of this problem, and these figures don't account for the vast numbers of dogs we suspect are being illegally trafficked into the country in addition to these."
Should we import from abroad?
According to a survey conducted via Savanta Comres on behalf of the RSPCA in 2020, 52% of UK dog owners surveyed agree that puppies and dogs should not be imported from other countries outside the UK under any circumstances.
Furthermore, 69% of UK adults agree that there should be greater control on how many imported dogs are allowed into the UK.
This was further supported by the fact that a poll run by Veterinary Voices UK showed that 98.8% of veterinary professionals polled would not recommend importing a dog from abroad.
Veterinary professionals in the poll were worried about the risk of imported diseases spreading to other animals, including other pets and livestock (in the case of some foreign parasites). They were especially concerned that zoonotic diseases (those that can spread from animal to human) could infect people coming into contact with the animals. Additionally, the severe emotional and behavioural distress many of these animals go through when being transported to the UK is of huge concern. There are also reports of veterinary behaviourists being inundated with requests from owners of foreign imports who are struggling with behavioural issues. In a poll on Veterinary Voices UK, 96% of veterinary professionals reported an increase in behaviour issues, largely in imported dogs.
Brucella canis: Why are we worried?
Brucella canis is a growing concern amongst UK veterinary professionals because although we don’t currently have Brucella canis endemic in our native UK dogs, cases are more regularly being diagnosed in dogs imported from abroad, particularly from Eastern Europe and the numbers are growing.
Cases appear to be rising due to increasing numbers of untested imported dogs, some of which are infected. Due to mixing and breeding, the first cases of transmission between dogs in the UK have now occurred according to the AHPA report. It can make infected pets poorly but the symptoms are often subtle and vague. Symptoms such as a sore back or just a general malaise (being generally under the weather). Of greater concern, dogs can be infected and spread the bacteria without any signs at all.
How is it transmitted?
Brucella canis spreads predominantly via reproductive fluids. The risk of spread is particularly high if a pregnant bitch aborts a litter of puppies. Neutered dogs therefore pose a lower risk of transmission, but it does not eliminate risk. The disease can also be spread via blood, urine and saliva. People living with an infected pet will have prolonged exposure to these fluids and are therefore more at risk if in regular and direct contact with the infected dog.
Reproductive
The predominant routes for dog-to-dog transmission are through coitus (sexual intercourse) and by vertical transmission from the dam (mother) to offspring. In particular, the aborting dog presents a significant risk for the spread of infection as large numbers of organisms are present in placental tissues, fluids, and aborted foetuses/stillborn puppies, with persistent shedding in vaginal discharge for at least 4–6 weeks. Products associated with abortion and parturition contain high levels of Brucella canis and are highly infectious for dogs and present the highest level of risks to dog owners and breeders (veterinarians and laboratory technicians may face other high risks via contact with infectious tissue and inadvertent culture of Brucella for example).
Non-reproductive disease transmission
The epidemiological significance of non-reproductive disease transmission is not well understood and the relative risk this route presents overall is unclear; however, it is known to occur and the risk is likely cumulative, being a function of the time spent with and the proximity to an infected dog, clearly a risk for those people living with or in frequent contact with a positive animal. In particular, transmission between dogs via urine is thought to be a significant route of infection within dogs living in the same accommodation.
Dogs may also become infected via direct contact with:
Oronasal and conjunctival mucosa
Broken skin
Secretions, excretions, and tissues (including blood) of infected dogs
Organisms are shed in milk, urine, and semen, and, at a far lower-level, saliva and tears
As well as direct contact, aerosolisation (particles small and light enough to be carried on the air) and fomite transmission through environmental contamination are alternative routes of infection, particularly within the kennel setting. Brucella canis organisms have also been detected inside ticks; however, the role of arthropod vectors in transmission is unknown.
Under favourable conditions (high humidity, low temperature, no direct sunlight, and absence of disinfectants), Brucella can survive for extended periods (months) in the environment, It can also survive frozen, including in semen and meat. This is why we should also be cautious when importing semen for artificial insemination if we do not know the health status of said stud dog. Brucella has also been transmitted in blood products, and in endemic countries risk assessment or screening of blood donors has been recommended, as we have the Pet Blood Bank in the UK, this is unlikely to be a common route for transmission but should be something to be aware of.
Signs of Brucella canis in dogs
Most dogs infected with Brucella canis are thought to remain subclinical, meaning they won't display any signs, however because of this these animals represent a significant reservoir of infection!
Clinical brucellosis classically manifests as a disease of canine reproduction (entire dogs) or as discospondylitis (bacterial infection of the intervertebral discs and vertebral bones) in entire and neutered dogs. The most common clinical manifestation of brucellosis in animals is reproductive issues; in female hosts include the birth of stillborn or weak offspring, retained placentas, decreased milk yield, and decreased fertility, while intact males experience orchitis (inflammation of the testicles), epididymitis (Inflammation of the epididymis), seminal vesiculitis, and testicular atrophy (progressive degeneration or shrinking of the testicles) in later stages. While reproductive failure is a hallmark of brucellosis, in many human and animal cases the diagnosis of brucellosis is complicated by a slow and insidious progression, characterised by very vague and nonspecific clinical signs such as lethargy, malaise, musculoskeletal pain, anorexia, and weight loss.
Nonspecific clinical signs not related to reproductive failure in dogs may include lethargy, weight loss, lameness, and exercise intolerance, along with findings of lymphadenopathy (swollen or enlarged lymph nodes) or splenomegaly (enlarged spleen).
Following intermittent episodes of bacteremia (bacterial infection in the blood) beginning 7 to 30 days after infection, Brucella canis may travel hematogenously (via blood stream) to the intervertebral disc, eye, or meninges, manifesting as uveitis (swelling of the uvea), granulomatous chorioretinitis and discospondylitis, or sacroiliitis (inflammation of one or both of the immovable joints formed by the bones of the pelvis called sacrum and the ilium). Dogs with discospondylitis often present with intermittent back pain, intermittent lameness, paresis (muscle weakness), and lethargy.
Signs of Brucella canis in people
Due to the zoonotic nature (can spread from animals to humans) of brucellosis, its management requires the awareness of medical professionals in both the human health and veterinary sectors, including knowledge of the exposure risks, diagnostic limitations, treatment practices, and preventative surveillance programs in place.
Transmission to humans is most likely to occur through contact with infectious canine reproductive tissues and discharges. Contact with urine, faeces, or saliva from infected dogs may also pose a risk. Additionally, laboratory personnel may be exposed through inhalation of infectious aerosols during manipulation of specimens.
Humans infected with Brucella canis may develop nonspecific signs such as intermittent fever, fatigue, and lymphadenopathy (swollen lymph nodes). Rarely, human infections result in more severe disease manifestations such as polyarthritis, meningitis, or endocarditis.
One review found that arthralgia (discomfort, pain or inflammation arising from any part of a joint including cartilage, bone, ligaments, tendons or muscles) was the most common reported symptom followed by pyrexia (fever), fatigue, hyperhidrosis (excessive sweating), and inappetence.
Clinical signs that were significant upon examination were pyrexia, hepatomegaly (enlarged liver), splenomegaly (enlarged spleen), peripheral arthritis, and hepatosplenomegaly (enlarged liver and spleen).
Unfortunately, this report did not distinguish between B. canis and other Brucella species. In the literature, however, there are multiple reports of human clinical infection with B. canis, which generally follows a similar course, although healthy and non-pregnant adults appear to be relatively resistant to severe disease. The main symptoms reported with B. canis infection are undulant fever, malaise, and splenomegaly. However, there are other complications.
In children, B. canis has been reported to cause significant respiratory disease and dyspnoea; while in adults, an association with Guillain Barré syndrome has also been reported.
Thankfully, human case-fatality proportion is very low; however, rare but severe complications of B. canis infection include the development of endocarditis and septic arthritis. The risk of endocarditis is probably around 2% of clinical cases, but is responsible for 80% of the fatalities for brucellosis in general. Moreover, following B. canis infection, risks of osteomyelitis, aneurisms and epidural abscessation, as well as skin lesions, are also recognised.
Overall, we can conclude that B. canis infection in humans is poorly understood, and behaves slightly differently from other Brucella species, but nevertheless represents a potential zoonotic threat. Children and the immunocompromised appear to be at the most risk, but much of the research is in the early stages, and seems to be complicated by underdiagnosis.
How do you diagnose it?
Brucellosis can be diagnosed with blood tests, which should be performed before any dog is imported and then repeated once they are in the UK. This is because if a dog is exposed to the bacteria, it can take a while for that to show up on tests. It can take up to 3 months to seroconvert meaning a dog may test negative for a number of months before testing positive. So, whilst one negative result is good, two are better. Your vets may ask to repeat the blood test around 3 months after your dog has entered the UK, in case they were exposed shortly prior to transport, for the safety of their team.
Unfortunately, once a dog is infected with Brucella canis, the infection can never be cleared, and the dog may continue to be infectious to others. Although treatment with antibiotics is possible, they will never fully clear the infection and the dog could begin to spread the bacteria again at any time.
Testing
No test can determine infection status with 100% accuracy. Test results must always be considered alongside additional evidence, such as clinical signs, movement history and infection status of contact and related dogs (e.g. siblings, parents and dogs the individual has mated with or been in close contact with when giving birth or aborting) in order to determine the infection status of the dog in question. Knowledge of tests and the specificity and sensitivity will help guide veterinary professionals on their decision making.
Sensitivity and specificity: explainer
Sensitivity and specificity describe the accuracy of a test which reports the presence or absence of a condition.
When looking at a disease like brucellosis, individuals who have the condition are considered "positive" and those who don't are considered "negative", then sensitivity is a measure of how well a test can identify true positives and specificity is a measure of how well a test can identify true negatives.
Sensitivity is the true positive rate and is the probability of a positive test result, conditional on the individual truly being positive. Specificity, the true negative rate, is the probability of a negative test result, if the individual truly is negative.
Types of test for Brucella Canis
Culture
A positive culture for B. canis is considered definitive evidence that the dog is infected. However, it is rarely achievable except in materials from an abortion, or a vaginal swab shortly after whelping. In some cases, especially in the earlier (acute bacteraemic) phases of infection, it may be possible to achieve a positive culture from vaginal or semen samples; however, as the bacteria are only intermittently shed and are very difficult to grow in a laboratory, false negatives are very common.
Holding out for a positive culture result would therefore result in a high probability of missing many, probably the majority, of clinical cases.
PCR
The same problems that apply to culture apply to PCR - although the sensitivity of the technique is higher, there are still substantial false negatives, as the levels of bacterial DNA in the blood are typically very low. Some laboratories have made claims of 100% specificity with PCR (although these have NOT been confirmed), however, the sensitivity remains quite poor.
Serology
As a result, we are forced to rely upon serological tests. Unfortunately, the range of tests available, the literature surrounding their use, and the degree of standardisation is both vast and inconsistent. However, there are three major issues with serological tests for Brucella canis in particular.
False negatives due to slow seroconversion
False positives due to the limitations of the test
False positives due to cross reacting antibodies
In practice, points (2) and (3) are indistinguishable, and so will be considered together.
False negatives
The main problem is that while antibodies against B. canis are usually present within 2 weeks (as with most other bacterial infections), some dogs - especially puppies - may take up to 3 months.
This problem is relatively easily overcome by ensuring that any serological test is performed a minimum of 3 months after the last-known possible date of exposure to the pathogen. In practice, this means 3 months after importation in the majority of cases.
False positives
This is a more vexing problem, particularly for veterinary professionals in general practice who have to balance the risk of a genuine positive to the patient, the client, themselves and their team, against the possibility of recommending euthanasia to a patient who may not be carrying the infection.
Different tests have different degrees of specificity; the widely-used FASTest patient-side tests (using a lateral flow system) have a claimed specificity of 90.7%. While this sounds good, given the apparently low prevalence of B. canis in imported dogs, it means that most positive results in apparently healthy dogs will in fact be negative. See below for the mathematics and some recommendations.
There are more specific tests available, specifically the iELISA and serum agglutination test (SAT) used by the APHA. It is strongly recommended to use these tests together; collectively, they have a reported specificity of 99%.
The False Positive Problem
The issue is that, at the moment, there appears to be a very low prevalence of B. canis in imported dogs. Reports suggest values ranging from 1.6% to 1.7%, but it is unclear whether the lower estimate has factored in the risk of false positives (the higher estimate did, but came from a relatively unhealthy population, who may have been at higher risk of carrying a range of infectious diseases). It is, however, appropriate to use the 1.6% value as a reasonable estimate of the true prevalence until more detailed further studies are carried out and (hopefully) published.
The geeky bit
The mathematics are relatively straightforward, the relevant formula being:
Specificity = True Negatives / (True Negatives + False Positives)
We can rearrange this to:
False Positives = (True Negatives / Specificity) - True Negatives
Once we have calculated the numbers of False Positives, we can then calculate the Positive Predictive Value - in other words, the proportion of those dogs who test positive who actually have the disease:
Positive Predictive Value = True Positives / (True Positives + False Positives)
For the patient-side FASTest, we can therefore calculate that for 100 imported dogs, 1.6 can be estimated to have B. canis, while 98.4 would not. The specificity is 90.7% (0.907).
Using our formulae gives us:
False Positives = (98.4 / 0.907) - 98.4 = 10.09
PPV = 1.6 / (1.6+10.09) = 13.7%
So, using the FASTest, only 13.7% of those dogs who test positive with a patient-side test kit actually have the disease - 86.3% do not.
We would therefore NOT recommend using the patient-side test kit to determine whether or not a dog is actually infected.
For the APHA test combination, we can calculate using those same figures, but this time with a 99% specificity:
False Positives = (98.4 / 0.99) - 98.4 = 0.99
PPV = 1.6 / (1.6+0.99) = 61.6%
So, in this case, 61.6% of those who test positive using the APHA combined test actually have the disease, and “only” 38.4% do not. Much better - but still not great!
A possible way forward
In an ideal world, of course, we would use these tests in series. So, initial screening with a patient side test would give us a subpopulation in which the true positive rate is 13.7%. By waiting 4-6 weeks, we can minimise the chance of accidentally picking up any other antibody response that only coincidentally contains cross-reacting antibodies.
We then resample and retest those dogs using the APHA protocol, giving us the following calculation (as we know that the true negative rate is 86.3%, from our earlier calculation using the FASTest figures):
False Positives = (86.3 / 0.99) - 86.3 = 0.87
PPV = 13.7 / (13.7 + 0.87) = 94.0%
By using a two-stage test (as Wright et al. did in their paper earlier this year), we can reduce the risk of false positives to less than 6%. Still not perfect, but dramatically better than the alternative.
Of course, subtle differences in the rate of true positives, and in the actual specificity of the tests, will result in wildly different results. However, at this time, this is the best data widely available - being cited even by those who disagree with the testing protocol - and we believe that it is helpful for colleagues and animal owners facing these decisions.
However, we hope that it also makes clear the risks implicit in accepting any single B. canis result as given, without considering the wider implications of false positives.
Treatment
Sadly, treatment is not recommended. While spontaneous recovery from Brucella canis is potentially possible in 1 to 5 years in some cases, other dogs remain chronically infected for life. Therefore, attempting to treat with antibiotics is not recommended, as it will not clear the infection and risks driving antibiotic resistance.
Neutering can help to reduce the Brucella canis transmission risk, but again, does not fully prevent it. Although neutering of infected dogs does not eliminate infection, it can prevent transmission via reproductive means (i.e. via coitus, exposure to products of abortion/parturition, or vertical transmission - spread from dam to pup). Furthermore, it is thought to reduce the risk of horizontal transmission (adult dog to adult dog) by decreasing the level of shedding and improving the response to antimicrobials, by reducing the volume of potentially infectious tissue.
The only way to fully eliminate the risk to humans and other dogs is, sadly, to euthanise them. This is of course a decision veterinary professionals do not take lightly, euthanasia can have a serious emotional toll on the professionals and pet owners themselves. However, dogs in the UK with brucellosis, where it is not endemic, pose an ongoing risk to other pets and people they come into contact with. It is very difficult (in fact, practically impossible) to cure an infected dog, and some pets will, sadly, become unwell with the disease. If they are suffering from disease caused by Brucella canis then euthanasia is an appropriate decision.
This is a tragic decision for any family to have to make but can be the kindest one for both the dog and their new owners. Vets do not wish to see anyone have to make that awful choice, which is one of the reasons why they are so concerned about the practice of importing dogs from abroad, particularly with the lack of testing we are seeing and the lack of information importing organisations are giving new owners about this disease.
Top Tips for Veterinary Practices:
Wear Personal Protective Equipment (PPE) when handling imported dogs or dogs with questionable travel status. Risk of transmission is low unless handling high risk body fluids such as reproductive fluids, abortive material etc
Remember that illegal smuggling is resulting in pregnant females being brought into the UK, so puppies may appear to be ‘UK born’ but are in fact still at risk of carrying the disease
Barrier nurse the patient to avoid any bodily fluid contamination for both personnel and other patients
Test the dog BUT be aware the the sensitivity and specificity of the test
If you get a positive result, do not panic. Take appropriate samples to send for confirmatory testing if required. Continue to use PPE. Discuss with the owner the risks involved in the disease, the likelihood that the patient does have the disease (given the test you used) and the implications going forward.
Ensure the dog is not coming into contact with any immunocompromised individuals or children
Ensure the dog is isolated from other dogs until test results are confirmed
If you feel that import documentation is not legitimate, re-test
Re-test dogs >3months after entering the UK due to seroconversion
NB: This article is an overview of Brucella Canis in the UK, it is not the advice of any organisation, but aims to investigate the evidence base and guide practices to make individualised risk assessments.
References and further reading:
Canine Brucellosis: Insights Into the Epidemiologic Situation in Europe
First Case of Human Brucella canis Infection in the Netherlands
https://www.nwlabs.co.uk/brucellosis-in-imported-dogs-an-important-update/
Comparisons of brucellosis between human and veterinary medicine - PMC (nih.gov)
Sensitivity and specificity explained: A Cochrane UK Trainees blog
FASTest Brucella Canis Diagnostic Test Kit | Vetlab Supplies Ltd
Zoonoses and veterinary public health: disease surveillance reports
Published16 June 2023
HAIRS risk assessment
Published 18 September 2023