Tackle ticks: the changing face of canine tick-borne disease

^{Images (L-R): Starover Sibiriak, Smith1972 & Erik Karits/Shutterstock.com}

^{Ian Wright BVMS.Bsc. Msc. MRCVS}

^{Veterinary surgeon, co-owner of the Mount Veterinary Practice.
Independent Parasitologist and head of ESCCAP UK & Ireland.}

Lyme disease has zoonotic potential and confirmed human cases continue to increase in the UK year on year. The incidence of canine disease is less clear but dogs across the country are being exposed to infection. Ixodes spp. ticks which carry B.burgdorferi are endemic in the UK and have a seasonal peak in numbers in spring and autumn months. While these peaks still occur, ticks are now commonly seen all year round throughout the UK (Smith et al., 2011) providing the potential for dogs and people to be exposed to infection throughout the year. This has led to the risk of a dog encountering an infected tick in the UK being approximately 1 in 200 over each tick season (Smith et al., 2012).

In addition to these increased risks of tick-borne disease exposure, these pathogens and the disease they cause have had significant media exposure. There have been a number of high profile Lyme disease cases in the media, and the outbreak of babesiosis in Essex reached the national news (e.g. http://www.bbc.co.uk/news/science-environment-35815813).

As a result of increased cases, media exposure and pet travel, veterinary professionals are likely to face increasing numbers of enquiries regarding the risk that tick-borne diseases pose, both to dogs and their owners. Therefore there is a need for veterinary professionals to give accurate advice to clients whose lifestyle puts them at particular risk. It is also vital that there is increased awareness of tick-borne disease and vector distribution, both in the UK and across Europe. This article provides a review of the epidemiology of canine tick-borne disease endemic in the UK, and those that might be encountered abroad.

• VIDEO CONTENT: Click to view videos showing tick acquisition of a host, attachment and emergence.

 

Key words: tick-borne disease, epidemiology, climatic effects, travelling pets

Endemic tick-borne disease in UK – Lyme disease

Lyme disease is caused by spirochete bacteria of the Borrelia burgdorferi complex and is transmitted by Ixodes spp. Although infection occurs in a wide variety of mammals, canines and humans seem particularly susceptible to the disease.

The sheep tick Ixodes ricinus (Figure 1) is the most important vector throughout Europe, including the UK, but I.hexagonus and I.canisuga may also play a significant role as UK vectors.

Lyme disease is maintained in endemic regions by two types of host.

• Reservoir hosts – act as subclinical carriers of infection and may therefore maintain its presence even in the face of reduced tick numbers and adverse conditions for the vector.
• Reproductive hosts – do not carry infection but maintain populations of infected ticks.

Small rodents and birds act as significant reservoir hosts in terms of maintaining infected tick numbers, whereas deer are important in terms of moving Lyme disease rapidly to previously uninfected parts of the country. An example of this is roe deer that have enabled rapid spread of infection through the Wye valley and into Wales (Böhm et al., 2007).

Ticks are commonly infected as larvae and then remain infected as nymphs and adults. When ticks feed, Borrelia spp. multiply in the gut and over a period of several days, penetrate the gut epithelium, migrate to the salivary glands and then can be potentially delivered to a new mammalian host. As a result, it is thought that transmission in most cases takes at least 24 hours to occur after attachment.

Faster transmission has been demonstrated under experimental conditions (Piesman et al., 1987, Piesman 1993, Shih & Spielman 1993) but only in mice models using Ixodes scapularis, which is not present in the UK. Even under heavy challenge in mouse models, the majority of transmission still takes at least 24 hours to occur.

Nymphs are thought to be the most significant stage in terms of overall transmission, due to their relative abundance compared to other tick life stages. They are also less likely than adults to be groomed off by pets due to their small size and more likely to be missed by owners checking their pets and themselves for ticks.

• VIDEO CONTENT: Click to see short videos on the tick blood meal and disease transmission.

Epidemiology – Lyme disease in dogs

Data concerning the current incidence of Lyme disease and prevalence of Borrelia spp. in dogs is lacking and there is a significant gap in our understanding of canine Lyme disease.

A small study of dogs and cats with clinical signs possibly associated with Lyme disease was carried out by Shaw et al. (2005). PCR analysis was used to determine the prevalence of tick-transmitted infections in 120 systemically ill dogs and 60 cats recruited over a period of three months from 52 veterinary practices in the UK. B. burgdorferi was detected in five dogs and two cats but there were no statistically significant associations between the infections and the clinical signs shown.

The PDSA recently published figures suggesting a massive increase in reported cases at their surgeries over a seven-year period, but these were suspected as well as confirmed cases, and should be interpreted in the light of increased awareness and reporting over that time period.

The distribution and prevalence of ticks infesting domestic dogs across the UK, however, has been examined (Smith et al., 2011), as well as the prevalence of B.burgdorferi in these ticks (Smith et al., 2012). 173 veterinary practices were recruited to monitor tick attachment to dogs between March and October 2009. A total of 3,534 dogs were examined and 810 dogs were found to be carrying at least one tick. Ixodes ricinus was identified in 72.1% cases, Ixodes hexagonus in 21.7% and Ixodes canisuga in 5.6%. The estimated incidence of tick attachment was 0.013 per day in March (lowest) and 0.096 per day in June (highest).

The prevalence of B.burgdorferi was examined in 739 of the ticks collected using PCR. 2.3% of the ticks tested were positive giving an overall prevalence of infected ticks on all dogs of 0.5%. This suggests that pet dogs are exposed to significant Borrelia spp. in the UK tick population. How this translates into prevalence of canine infection and incidence of disease remains unknown but the prevalence in attached ticks means that dogs walking in rural areas or those with a history of regularly acquiring ticks should be considered at significant risk.

Lyme disease is currently rarely recognised in cats but it is unknown whether this is due to cats being relatively resistant to exposure, resistant to disease or whether it is under-reported and diagnosed in felines.

Epidemiology – Lyme disease in the UK human population

The reported incidence of human Lyme disease in the UK is increasing year on year. There were 0.5 cases per 100,000 people in England and Wales in 2001. This had risen to 1.73 cases per 100, 000 in 2011.

In 2010 there were 953 reported cases in England and Wales but, with considerable under-reporting likely, the number of cases was probably nearer to 3,000 (Health Protection Agency, 2011). Public Health England (PHE) has published figures showing that 421 cases of laboratory confirmed cases of Lyme disease were diagnosed in the UK during the third quarter of 2015. In comparison, 300 were reported during the same time period in 2014.

The growing number of reported cases is likely to be partially due to a genuine increase in disease transmission, as well as heightened awareness among the general public and the medical profession concerning the disease. A number of high profile celebrity cases reported in the British press is likely to have added to this public concern.

The arrival of infected migrants to the UK from Eastern Europe, where the incidence of Lyme disease is higher has been postulated as a reason for the increase in the incidence of Lyme disease (O’Connell et al., 1998) but is probably not a significant factor in recent years as migration has not increased in this time period at anywhere close to the rate of increase of reported Lyme disease cases. A genuine increase in transmission is more likely to be being driven by increased outdoor recreational activity and an increase in wild host reservoir or tick numbers.

It has been suggested that dog owners might be at a greater risk of infection from Lyme disease than people without dogs but there is no evidence to support this and infected dogs pose little or no direct risk to humans (Goosens et al., 2001). Dog owners can therefore be reassured they are at little direct risk if their pet has Lyme disease or is carrying Borrelia spp. infection but they may also be exposed to infected ticks while walking their dog.

Dermacentor reticulatus and babesiosis in the UK – a vector looking for a disease

Babesiosis is a tick-borne disease caused by a variety of Babesia spp.

Babesia spp. are described by their shape in red blood cells (piroplasms) and their size in relation to the red blood cell (large or small). There are four Babesia spp. in Europe that can infect dogs, two large (Babesia canis canis and Babesia canis vogeli) and two small (Babesia annae and Babesia gibsoni).

The most pathogenic is the large Babesia canis canis and its distribution is closely linked with its main vector, D.reticulatus. Although this tick is present in endemic foci in the UK, until recently the UK had remained free of babesiosis other than in travelled dogs. Increased pet travel and a viable vector present in the UK meant that the risk of introduction of B.canis canis was high, and concerns about its introduction came to fruition with the outbreak in Harlow, Essex.

Life cycle and transmission

Infection occurs when the parasite is transmitted in the saliva of a feeding tick, occurring 24-48 hours after the start of feeding (Matjila et al., 2004). Sporozoites in tick saliva enter blood cells where they form merozoites and multiply. The red blood cells then rupture, releasing the merozoites, that then go on to invade other red blood cells. Ticks are infected during feeding.

Following ingestion by the tick, Babesia undergoes sexual reproduction and asexual multiplication, leading to sporozoites being present in the tick salivary glands. Sporozoites are then transmitted to new hosts through the tick’s saliva.

Migration to the tick’s ovary also occurs leading to vertical transmission. This allows rapid spread of the parasite in tick populations and also means that tick larvae and nymphs can be important sources of infection.

Transmission of infection has also been reported through blood transfusions and in the case of B.gibsoni, through dog bites (Jefferies et al., 2007).

Babesiosis in Europe

Babesia canis canis is the most widespread and pathogenic of the Babesia spp. in Europe. Its distribution is closely tied to its vector, Dermacentor reticulatus (Figure 2), and it is endemic in northern Spain, Portugal, France and Italy.

The incidence of babesiosis caused by B.canis canis is increasing, which is of concern as these are popular tourist destinations. It is also consolidating its range, with endemic foci in central and eastern Europe, spreading up to the Baltic region.

Even in endemic regions, Dermacentor inhabits specific ecological niches such as marshland, sand dunes, river and pond banks and grassland on woodland paths, leading to dense endemic foci. This can lead to large numbers being suddenly encountered by pets or people and rapid establishment of B.canis canis in a new area once introduced.

Babesiosis in the UK

Although there had been a fatal case of babesiosis caused by B.canis canis in an untravelled dog in the UK (Holm et al., 2006) it was not thought to be endemic. D.reticulatus, however, has established endemic foci in Essex and Wales, creating the possibility of B.canis canis becoming established in these ticks. The fear had been that this would become more likely as increased pet travel increased the risk of introducing B.canis canis, either through infected pets or ticks.

This fear became reality when in February 2016, B.canis canis was reported in three dogs from Harlow, Essex (Swainsbury et al., 2016), followed by a fourth dog from the same area in March 2016 (Woodmansey, 2016). The four dogs were from four separate households, had not travelled abroad and had not been in contact with dogs that had done so (Woodsmansey, 2016). DNA barcode testing and PCR testing confirmed ticks found on the infected dogs to be Dermacentor reticulatus infected with B.canis canis (Phipps et al., 2016). This suggests that there is now an endemic focus of B.canis canis in Essex and this pocket of infection is likely to spread.

Transovarial transmission from tick to tick has the potential to rapidly increase B.canis canis prevalence in the tick population. Infected ticks are also likely to be disseminated on mammalian hosts, mechanically in vehicles and on clothes.

It is difficult to predict where and when the parasite will spread in the country, as it is unknown where other Dermacentor foci may be. Even within endemic areas, the patchy nature of the tick in environmentally favourable niches means that it may take time to spread but then rapidly establish in a new area if a dense focus of ticks is infected.

It has been suggested that relaxation of the compulsory treatment for ticks before return to the UK under the Pet Travel Scheme (PETS) was in some way responsible for D.reticulatus becoming endemic in the UK. This tick was present in the UK, even before the relaxation of the rules but it is likely that increased pet movements overall have led to the spread of B.canis canis across Europe, and now to the UK.

The other large Babesia spp. is Babesia canis vogeli. It is transmitted by Rhipicephalus sanguineus, and while common in Southern Europe, is of relatively low pathogenicity.

Cases of babesiosis caused by the small Babesia spp. Babesia annae and Babesia gibsoni are sporadic but B.gibsoni can potentially be transmitted by Ixodes spp. ticks. Smith & Wall (2013) tested 742 ticks found on dogs by PCR for Babesia spp. and found 16 (2.4%) were positive for Babesia spp. and of these 11 showed 97-100% homology with B.gibsoni. Although B.gibsoni is not as pathogenic as B.canis canis, these results suggest that B.gibsoni may already be endemic in the UK; but further work is required before the epidemiological significance of this is known.

Rhipicephalus sanguineus and the risk of tick-borne disease associated with pet travel

Rhipicephalus sanguineus is not currently endemic in the UK as the climate is not favourable for establishment of an endemic population at present. The tick is predominantly endemic in Southern Europe (Figure 3) due to its preference for a warm climate but is thought to be moving northwards into central European countries, including France. This makes the potential establishment of endemic foci in the South a concern. It has the potential to complete its life cycle more quickly than Ixodes spp. ticks, often within one season. This allows it to potentially take advantage of centrally heated homes and become established in households in a similar way to fleas.

Two cases of such household infestations have recently been recorded in the south of England (Hansford et al., 2015). These cases were from dogs that had been imported from Europe and at least one had been tick treated before admission. Nymphs of R.sanguineus survived and once established took more than 12 months to eliminate, despite effective tick treatment of dogs within the household and repeated fumigation of the house.

In addition to the potential for house infestation, R.sanguineus is also the vector for a number of tick-borne diseases that are a concern for travelling and imported dogs, but would also potentially form endemic foci in the UK if R.sanguineus were to become established.

• Canine monocytic ehrlichiosis – can cause acute febrile disease or a more dangerous chronic form to the patient. It is caused by Ehrlichia canis. Countries with reported infections in dogs include France, Italy, Portugal, Spain and Greece, in line with distribution of its R.sanguineus vector. Reported cases in untravelled dogs in Germany and Switzerland, however, have fuelled suspicions that R.sanguineus is increasing its range.
• Hepatozoonosis – caused by the rickettsia Hepatozoon canis. This pathogen is transmitted by ingestion of ticks while grooming and infection can be fatal. It is often present in mixed infections, however, and it can be difficult to attribute specific signs to H.canis infection. It is found in Southern and Western European countries, including France, Spain, Portugal and Italy.
• Mediterranean spotted fever (MSF) – is an acute zoonotic disease, which may also rarely clinically affect dogs, caused by Rickettsia conorii. This zoonotic pathogen was the driving force behind the compulsory tick treatment on the Pet Travel Scheme before return to the UK, as it is capable of causing significant complications in human patients. Compulsory tick treatment was dropped, primarily on the grounds that R.conorii is thought to be limited to Southern Europe and that R.sanguineus is unlikely to become established in the UK and Scandinavia due to the colder climate of these countries. Its distribution in southern Europe is far from certain, as many infected dogs will be sub-clinical carriers. This makes vigilance for R.sanguineus ticks entering the UK vital, to alert veterinary professionals to the possibility of this infection being present in dogs having travelled in Europe, but also, to prevent transmission.
• Canine cyclic thrombocytopaenia – caused by the platelet-inhabiting Ehrlichia platys. Its distribution closely follows that of R.sanguineus with infection and clinical disease being observed in many southern European countries, including France, Italy, Portugal, Spain and Greece.

Prevention of tick-borne disease in dogs

Prevention of exposure to tick-borne disease in dogs is a three-stranded approach.

1. Daily monitoring for ticks – and careful removal of ticks with a tick hook within 24 hours of attachment. A simple “twist and pull action” is required. This can also be performed with tweezers but they should be fine pointed and not blunt, as crushing will stress the tick, causing it to expel stomach and salivary gland contents, increasing the risk of disease transmission. Traditional techniques to loosen the tick such as the application of petroleum jellies, freezing or burning will also increase this likelihood and are contraindicated.
2. Chemical tick prophylaxis – On current evidence, tick-borne pathogens endemic in the UK take at least 24 hours to transmit. Therefore, for dogs considered to be at risk of exposure to ticks and tick-borne diseases, a preventative product should be recommended that will rapidly kill or repel ticks. No tick preventative product is 100% effective but the isoxazolines and pyrethroid-containing products are highly efficacious for this purpose. Compliance and lifestyle should be considered, such as preference for a tablet, spot-on preparation or collar, as well as previous product reactions and frequent exposure to water/shampoo. When travelling abroad a repellent pyrethroid product should be selected where possible. This is essential in southern Europe to reduce the transmission of Leishmania infantum, but also to reduce Rickettsial parasite transmission such as E.canis which may be transmitted within a few hours of biting (Fourie et al., 2013).
3. Vaccination – A licensed vaccine is now available for Lyme disease prevention (Merilym 3). The vaccine prevents migration of the spirochete to the salivary glands, reducing the risk of infection as a result.

Preventative measures should be recommended for all dogs travelling abroad and repellent products applied a week before travel. In the UK, whether chemical prophylaxis and vaccination are justified should be based on individual risk.

Other factors, such as compliance and the level of concern displayed about tick-borne disease by the owner, should also be considered.

Management of zoonotic risk

Zoonotic risk from Lyme disease (and R.conorii when travelling abroad) comes from exposure of people to infected tick bites. Avoiding high tick and Lyme disease endemic areas is the most effective way of minimising risk but these are also some of the most popular walking and outdoor recreational sport destinations in the country.

Sensible precautions when travelling in these areas include: wearing long sleeves and ensuring the lower body is covered; the use of repellent sprays on the body or clothing and careful inspections for ticks on the body after periods spent outdoors.

Local councils will often put up signs in high risk areas, giving some or all of this advice (Figure 4).

Conclusions

Tick-borne diseases are a growing threat to UK dogs, both in terms of increased potential exposure to B.burgdorferi and B.canis canis and pet travel.

Increased vigilance as to the distribution of tick-borne pathogens and their vectors, as well as increased awareness of the diseases they may cause is vital if disease rates are to be reduced and if the introduction of new diseases into the UK is to be avoided.

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References and further reading

• Böhm, M, White, PC, Chambers, J, Smith, L and Hutchings, M (2007). Wild deer as a source of infection for livestock and humans in the UK. The Veterinary Journal 174: 260–76.
• Fourie, JJ, Stanneck, D, Luusa, HG, Beugnet, F, Wijnveld, M et al. (2013). Transmission of Ehrlichia canis by Rhipicephalus sanguineus ticks feeding on dogs and on artificial membranes. Veterinary Parasitology 197: 595–603.
• Goosens, HAT, Van Den Bogaard, AE and Nohlmans, MKE (2001). Dogs as sentinels for human Lyme borreliosis in the Netherlands. Journal of Clinical Microbiology 39: 844–8.
• Hansford, KM, Pietzsch, M, Cull, M and Medlock, JM (2015). Brown dog tick infestation of a home in England. Veterinary Record 176: 129–30
• Health Protection Agency (2011). Epidemiology of Lyme borreliosis in the UK.
• Holm, LP, Kerr, MG, Trees, AJ, McGarry, JW, Munro, ER, Shaw, SE (2006). Fatal babesiosis in an untravelled British dog. Veterinary Record. 159: 179–180.
• Jefferies, R, Ryan, UM, Jardine, J, Broughton, DK, Robertson, ID, Irwin, PJ (2007). Blood, Bull Terriers and Babesiosis: further evidence for direct transmission of Babesia gibsoni in dogs. Australian Veterinary Journal. Nov; 85(11): 459–63.
• Matjila, PT, Penzhorn, BL, Bekker, CP, Nijhof, AM and Jongejan, F (2004). Confirmation of occurrence of Babesia canis vogeli in domestic dogs in South Africa. Veterinary Parasitology 122: 119–25.
• O’Connell, S, Grantrom, M, Gray, JS and Stanek, G (1998). Epidemiology of European Lyme borreliosis. Zentralblatt fur Bakteriologie Mikrobiologie und Hygiene Series A. Medical Microbiology Infectious Diseases Virology Parasitology 287: 229–40.
• Phipps, L, Del Mar Fernandez De Marco, M, Hernández-Triana, L, Johnson, N, Swainsbury, C et al. (2016). Babesia canis detected in dogs and associated ticks from Essex. Veterinary Record 178: 243–4.
• Piesman, J, Mather, TN, Sinsky, RJ and Spielman, A (1987). Duration of tick attachment and Borrelia burgdorferi transmission. Journal of Clinical Microbiolology 25: 557–8.
• Piesman, J (1993). Dynamics of Borrelia burgdorferi transmission by nymphal Ixodes dammini ticks. Journal of Infectious Disease 167: 1082–5.
• Shaw, SE, Binns, SH, Birtles, RJ, Day, MJ, Smithson, RC et al. (2005). Molecular evidence of tick-transmitted infections in dogs and cats in the United Kingdom. Veterinary Record 157: 645–8.
• Shih, CM and Spielman, A (1993). Accelerated transmission of Lyme disease spirochetes by partially fed vector ticks. Journal of Clinical Microbiology 31: 2878–81.
• Smith, F, Ballantyne, R, Morgan, E and Wall, R (2011). The prevalence, distribution and risk associated with tick infestation of dogs in Great Britain. Medical & Veterinary Entomology 25: 377–84.
• Smith, FD, Ballantyne, R, Morgan, E and Wall, R (2012). Estimating Lyme disease risk using pet dogs as sentinels. Comparative Immunology, Microbiology & Infectious Diseases 35: 163–7.
• Smith, FD and Wall, R (2013). Prevalence of Babesia and Anaplasma in ticks infesting dogs in Great Britain. Veterinary Parasitology 198: 18–23.
• Swainsbury, C, Bengtson, G and Hill, P (2016). Babesiosis in dogs. Veterinary Record 178: 172.
• Woodmansey, D (2016). New tick-borne disease confirmed in UK dogs. Veterinary Times 46.