Understanding Transmission of Infection by Ticks and New Strategies for Control
World Small Animal Veterinary Association World Congress Proceedings, 2008
Susan E. Shaw, BVSc (Hons), MSc, DACVIM, DECVIM-CA, FACVSc, MRCVS
Department of Clinical Veterinary Science, University of Bristol
Langford, North Somerset, UK

The current emergence, re-emergence and geographical spread of vector transmitted diseases are major concerns for human and animal health. There are many interacting factors responsible for the situation including climate change, increased contact of humans and domestic animals with infected vectors and reservoirs through ease of access to different bioclimatic areas. Current (and predicted) climate change resulting in warmer winters in northern Europe is favouring extension of tick and reservoir host activity later into autumn and earlier into spring. Human influence on habitat such as the forestry and park conservation, has resulted in increased density of host populations such as deer, at the same time as providing increased access for humans and animals. Consequently, understanding interactions between ticks, the pathogens they transmit and their vertebrate hosts is the subject of intense research. However, there is still scant knowledge about the transmission of the important tick-transmitted diseases affecting companion animals.

Ticks (sub-phyla Chelicerata) are obligate blood-feeders and many blood-borne microbial pathogens have co-evolved to take advantage of the arthropod's feeding behaviour and specialised mouthparts to by-pass the vertebrate host's cutaneous and vascular barriers. In addition, ticks themselves may become specialised 'biomes' for pathogen sequestration, replication and life cycle development. Tick-borne pathogens of importance in small animals include species of Babesia, Ehrlichia, Anaplasma, Rickettsia, Borrelia, Hepatozoon and Bartonella.

Pathogen Infection of Ticks

Ticks are adapted for relatively prolonged attachment to their hosts. The paired chelicerae penetrate the epidermis and macerate dermal capillaries, and the toothed hypostome in combination with secretion of specialised cement holds the mouthparts in place during repeated feeding and salivary injection. Pathogens adapted to tick-transmission are ingested in host blood or skin tissue fluids by ticks, and then penetrate gut epithelium. Both these processes are not passive and are potentially complex. Components of tick saliva may affect the success with which pathogens are ingested. Survival in the difficult environment of the tick gut requires pathogen/host adaptation, avoidance of the non-specific immune system, e.g., defensins and successful receptor attachment and penetration of the gut epithelial cells.

Pathogens are disseminated by the haemolymph and localise within various tick tissues including salivary epithelial cells and ovaries using specific receptors and avoiding immune-destruction. The exact sites and mechanisms of sequestration, and the dynamics of microbial infection in the tick host are poorly understood. Some microbial pathogens such as Borrelia burgdorferi preferentially adhere to the midgut epithelial cells until stimulated by a new blood meal to replicate and migrate via the haemolymph to the salivary gland. Others such as Babesia spp. and Rickettsia rickettsii target the salivary epithelial cells early after infection where they sequestrate. Infection is maintained through the tick moulting process (trans-stadial transmission) from one stage till the next. In this way, ticks remain persistently infected for long periods and pathogens are protected throughout detrimental climatic conditions until the next susceptible vertebrate host provides a blood meal.

In certain tick-pathogen relationships, particularly where systemic pathogen load is high and disseminated (e.g., Babesia canis), localisation and sequestration also occurs in the adult tick ovaries. This allows direct pathogen transmission (transovarial) to eggs and larvae.

Transmission of Infection to Vertebrate Hosts

In most cases, pathogen transmission from infected ticks occurs by injection of infected saliva through the tick bite wound. The process of attachment and feeding stimulates re-activation, replication and migration of pathogens from sites of sequestration to the saliva. The dynamics of this process are poorly understood in many tick-pathogen relationships and the time between attachment and infection of the tick bite site is unknown in many cases and if known, is variable between species (Table 1).

Table 1. Time between attachment and infection of tick bite site.

Species

Time to infection

Borrelia burgdorferi / Ixodes ticks

48-72 hrs, less in B. afzelli

Anaplasma phagocytophilum / Ixodes ticks

24-48 hrs

Babesia canis / Dermacentor ticks

48-72 hrs

Rickettsia rickettsii / Dermacentor ticks

5-20 hrs

Ehrlichia canis and other Ehrlichia species

unknown

Babesia gibsoni and other piroplasms

unknown

Pathogen transmission times are decreased if the tick feeding process is bypassed. Contamination of mucosal wounds with infected tick haemolymph may result in more rapid infection. If the tick feeding process is partially interrupted and the tick is allowed to attach to second suitable host, transmission times are also decreased.

Hepatozoon spp. are an exception to transmission through tick bites. H. canis is widely disseminated in tick tissues and host infection occurs following ingestion of infected ticks. Infective oocysts are released from tick tissue and in turn release sporozoites which penetrate the host gut epithelium and enter the lymphatics.

Strategies for Controlling Transmission of Tick-borne Pathogens

Tick Repellents

Synthetic pyrethroids, in particular permethrin, in on-animal topical preparations and impregnated into textiles for human use have been shown to effectively repel tick species that are commonly incriminated in transmitting pathogens. In general the use of repellents is limited by a short duration of action although significant tick repellent activity is reported up to 3 weeks after application of topical permethrin in dogs.

On-animal Acaricides

There are several safe, very effective acaricides with long-duration of activity across multiple tick species licensed for use in dogs (amitraz, fipronil, permethrin, pyriprole) and cats (fipronil). All are contact toxins and exert their lethal effects by interference with tick neurological function within 24 hours (permethrin) or 24-48 hours (amitraz, fipronil, pyriprole). It is possible that transmission of some pathogens (e.g., A. phagocytophium, B. afzelli, R. rickettsii) occurs before ticks are killed. However, the toxicity is accumulative and the neuromuscular activity required for feeding may be impaired even though attachment has occurred and well before tick death. There are no reported studies on the effect of sub-lethal acaricide concentrations on pathogen activation, replication, migration and salivary injection. Field efficacy studies of regular acaricide use in highly exposed dog populations strongly supports their role in decreasing the sero-prevalence of Borrelia spp., Babesia spp. and Ehrlichia canis.

Environmental Acaricides

Acaricides licensed for household use such as permethrin, can play an important role in a control strategy for Rhipicephalus-transmitted pathogens. This species is well adapted to domestic habitats (cars, kennels, houses) with all life cycle stages feeding on dogs. Environmental control of tick species that have sylvan life cycles involving wild-life hosts (e.g., Ixodes sp) is extremely difficult.

Mechanical Removal

Recognition of immature ticks is important as nymphs may be the most important stages for pathogen transmission. Regular brushing may prevent attachment or ingestion of ticks and is part of a combined strategy for control of hepatozoonosis.

Vaccination Against Ticks

Vaccination strategies have been devised to limit tick infestation and thus pathogen transmission. Despite there being many vaccine candidates, the only product available commercially is a recombinant Boophilus tick vaccine for cattle. Antibodies produced against the recombinant tick antigen Bm86 mediate lysis of tick gut cells when ingested in a blood meal. The decreased tick burden and fecundity produced as a result allowed reduction of acaricide therapy. Experimentally dogs have been vaccinated with a Freunds adjuvanted midgut extract from Rhipicephalus sanguineus. Subsequent tick challenge resulted in decreased attachment feeding time and fecundity.

Blocking Tick Attachment

Several tick salivary proteins have been identified that may be components of the cement that is essential for firm host attachment. A 29kDa protein has been cloned and immunisation of rabbits confers protection from tick bite.

Alteration of Dynamics of Pathogen Infection Within Ticks: The ospA/ospC Vaccine

Following ingestion by Ixodes ticks, B. burgdorferi upregulates production of a surface protein osp A (plus ospB) which then attaches to a tick midgut receptor (TROSPA). This ensures persistent adherence of the spirochete. When the tick next feeds, ospA is downregulated and ospC is upregulated. OspC facilitates borrelial migration, invasion of the salivary gland and adherence to salivary epithelial cells. Vaccines based on ospA or ospA/B have been developed. When anti-ospA antibody is ingested by the tick with the blood meal and binds complement in the tick gut, there is arrest of tick growth, impaired attachment and killing of spirochetes in the tick gut. In addition, animals with high levels of antibody to opsA are also protected against spirochete infection.

References

1.  Day MJ. Interaction of the host immune system with arthropods and arthropod-borne infectious agents. In Arthropod-borne Infectious Diseases of the Dog and Cat. SE Shaw; MJ Day Editors, Manson Publishing Ltd, London; 2005, 30-40.

2.  Hovius JWR, van Dam AP, Fikrig E. Tick-host-pathogen interactions in Lyme borreliosis. Trends in Parasitology. 2007, 23, 439-444.

3.  Tsuji N, Battsetseg B, Boldbaatar D. Babesial vector tick Defensin against Babesia sp Parasites. Infection and Immunity 75 (7): 3633-3640.

Speaker Information
(click the speaker's name to view other papers and abstracts submitted by this speaker)

Susan E. Shaw, BVSc(Hons), MSc, DACVIM, DECVIM-Ca, FACVSc, MRCVS
Department of Clinical Veterinary Science
University of Bristol
Langford, North Somerset, UK


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