Ticks and Disease in Kentucky, Entomology

Ticks and Disease in Kentucky

ENTFACT-618: Ticks and Disease in Kentucky | Download PDF | En Español

by Lee Townsend & Michael F. Potter, Extension Entomology
University of Kentucky College of Agriculture

Ticks are external parasites that must have three blood meals during their life in order to develop and reproduce. The common species in Kentucky that bite humans also feed on a range of animal species. Ticks feed slowly. During the several days needed to ingest a blood meal, they may pick up pathogens from infected hosts. Ticks can pass these disease agents to susceptible hosts during their next blood meal. Ticks are common; fortunately, the incidences of tick-borne diseases in the state are very low.

Significant increases in wildlife populations, expanded ranges of some tick species, development of housing in rural areas, and the popularity of hiking and ecotourism have increased the potential for people to encounter ticks. Awareness and use of preventive measures to reduce exposure while working outdoors or enjoying outdoor activities are keys to reducing tick bites. Use repellents and check yourself frequently for ticks while and after being in areas where they may be active.

Tick-borne diseases

Table 1. Main vectors of tick-borne diseases in Kentucky

Anaplasmosis is a bacteria disease that was recognized in humans in the mid-1990’s. Flu-like symptoms may develop 1 to 2 weeks after being feed upon by an infected tick. White-footed mice, short-tailed shrews, and eastern chipmunks are among the reservoir hosts of this disease.

Erlichiosis results from infection by one of several species of bacteria. Mild muscle aches, fatigue, and occasionally severe fever appear within 1 to 2 weeks after a bite by an infected tick. Ticks appear to have to feed for about 24 hours before disease transmission occurs. White-tailed deer, elk, and wild rodents are reservoirs of the disease.

Lyme disease is caused by a bacterium transmitted by the bite of infected blacklegged ticks. In most cases, the tick must be attached for several hours before transmission occurs. A characteristic bulls-eye rash may accompany the typical flu-like symptoms. If not treated, Lyme disease can spread to the heart, nervous system, and joints. White-footed mice are an important reservoir of the disease.

(1 dot placed randomly within county of residence for each confirmed case)

Red meat allergy may appear as a skin rash or anaphylactic reaction that occurs 3 to 6 hours after eating beef, pork, or lamb. The reaction can occur in people with a history of strong reactions to tick bites (redness and itching at bite sites that last for weeks) or many bites from a single incidence. They produce antibodies to proteins in the saliva of feeding lone star ticks. The common sugar (alpha-gal) that causes the reaction is not present in chicken, turkey, or fish. This antibody has been found in up to 20% of people tested who live where the lone star tick is common.

Southern tick-associated rash illness (STARI) produces a rash similar to that of Lyme disease along with flu-like symptoms (fatigue, headache, fever, and joint pain). STARI has not been linked to chronic joint, neurologic, or cardiac symptoms seen with Lyme disease. The cause of STARI is unknown; however, distribution of the disease coincides with the range of the lone star tick.

Spotted fevers (a group including Rocky Mountain Spotted Fever (RMSF) are bacterial diseases transmitted by infected American dog ticks. Typical symptoms include fever, headache, abdominal pain, vomiting, and muscle pain. A rash also may develop. Rocky Mountain spotted fever can be a severe or even fatal illness if not treated in the first few days of symptoms. Reservoir animals include deer mice, meadow voles, and other small mammals. Less than 1% of American dog ticks are likely to carry the pathogen, even in areas considered highly endemic. Dogs are susceptible to infection but the disease is rarely diagnosed in cats.

Tularemia (rabbit fever) is a rare but potentially fatal bacterial disease of rabbits, hares, and rodents; however, it can infect more than 100 species of wild and domestic animals. American dog ticks and lone star ticks can transmit the disease to humans. In addition, humans can contract tularemia when handling infected animals. Signs and symptoms vary with the method of entry into a person but a fever accompanies all forms. Cats and dogs may contract the disease by eating flesh of infected animals or through tick bites.

Avoiding Tick Bites

The best strategy to reduce the potential of contracting tick-borne diseases is to avoid tick bites. Here are some tips:

  • Avoid walking through uncut fields, brush and other areas likely to harbor ticks. Walk in the center of mowed trails to avoid brushing up against vegetation.
  • Use a repellent that contains 20 to 30 percent DEET on exposed skin. Always follow product instructions.
  • Use products that contain permethrin to treat clothing and gear, such as boots, pants (especially the cuffs), socks and tents.
  • Tuck long pants into your socks and boots. Wearing light-colored pants makes ticks easier to see.
  • In areas where there are ticks, check yourself, children and other family members for ticks every 2 to 3 hours and upon returning home from hikes and outdoor activities. Examine behind ears, hair, neck, legs and around the waist.
  • If you let your pets outdoors, check them often for ticks. Ticks can “hitch a ride” on your pets, but fall off in your home before they feed. Tick collars, sprays, shampoos, or monthly “top spot” medications help protect against ticks.

Removing an attached tick

In many cases, infected ticks must be attached and feeding for several hours before a pathogen is passed so prompt removal is very important.

How To Remove a Tick

Step 1: Use fine-tipped tweezers to grasp the tick as close to the skin’s surface as possible. the goal is to remove the entire tick including its head and mouth.

Step 2: Pull up with steady, even pressure. do not twist or jerk the tick.

Step 3: Clean the bite area and your hands with rubbing alcohol, an iodine soap, or soap and water.

A feeding tick holds itself in place by barbed mouthparts and a type of glue. Grasp it with fine-point tweezers as close to the skin as possible. Pull it straight out gently but firmly. Do not twist or jerk the tick during removal. Afterwards, wash the bite area and your hands thoroughly with soap and water and apply an antiseptic to the bite site.

You can store removed ticks in a sealed plastic bag with the date and location noted. Identification of ticks is available through your local Cooperative Extension Service office.

Testing Ticks for Disease

Anyone with concerns about exposure to ticks and possible disease transmission should consult their physician to determine the best course of action. Most tick-borne diseases can be averted by early intervention with an antibiotic.

Several laboratories will test ticks for selected diseases. Contact information is available at http://www.tickencounter.org/tick_testing/labs.

Here are some points to consider:

  • Testing ticks for disease is not a substitute for diagnosis by a physician. However, the results may be useful in deciding on the value of treatment in the absence of disease symptoms.
  • A positive test result for ticks does not mean that disease transmission occurred. An infected tick may not have fed long enough to transfer the pathogen.
  • Be sure that you understand the testing capabilities, costs, and proper shipping procedures for samples.

References

Centers for Disease Control – Rocky Mounty Spotted Fever https://www.cdc.gov/rmsf/index.html

Feldman, KA. 2003. Tularemia. JAVMA 222:725-730.

Keesing, F, MH Hersh, M Tibbetts, DJ McHenry, S Duerr, J Brunner, M Killilea, K LoGiudice, KA Schmidt, and RS Ostfeld. 2012. Reservoir competence of vertebrate hosts for Anaplasma phagocytophilum. Emerging Infectious Diseases 18:2013-16.

Stromdahl, EY and GJ Hickling. 2012. Aetiology of tick-borne human diseases with emphasis on the south-eastern United States. Zoonoses Public Health 59:48-64.

University of Rhode Island tick encounter resource center. http://www.tickencounter.org/

CAUTION! Pesticide recommendations in this publication are registered for use in Kentucky, USA ONLY! The use of some products may not be legal in your state or country. Please check with your local county agent or regulatory official before using any pesticide mentioned in this publication.

Of course, ALWAYS READ AND FOLLOW LABEL DIRECTIONS FOR SAFE USE OF ANY PESTICIDE!

entomology.ca.uky.edu

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Who, What, Why: How dangerous are tick bites in the UK?

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Walkers are being warned to protect themselves against tick bites after a wet and mild winter. Just how dangerous are ticks, asks Vanessa Barford.

Experts have warned that ticks — blood-sucking, disease-carrying arachnids — appear to be on the rise in the UK.

Richard Wall, professor of Zoology at Bristol University, says there’s no definitive data on how many ticks are in the country. Some areas have none. Others — usually woodland and heath areas — may have more than 100 per square metre. However, the general consensus among rural communities is they are on the up, largely as a result of the warmer and wetter weather (good breeding conditions) and the growing number of wild deer (ticks like living on their skin).

The answer

  • Ticks are on the rise in the UK
  • Lyme disease is too
  • It is treatable so long as it is caught early
  • Symptoms usually take between three days to six weeks to appear

The number of confirmed cases of Lyme disease — the most serious bacteria infection spread to humans by infected ticks — has also increased, according to Dr Tim Brooks, head of the Rare and Imported Pathogens Laboratory. He says laboratory proven cases have risen from about 200 in the late 1990s, to 1,200 last year, although the actual number of cases is probably three times that. Awareness and testing of the disease has also gone up, so the figures have to be seen in that context, he adds.

Lyme disease is treatable with antibiotics if it’s diagnosed early. But neurological problems and joint pain can develop months or years later if it’s left untreated. In the worst cases, it can be fatal.

The most common symptom is a pink or red circular «bull’s-eye» rash that develops around the area of the bite, but it doesn’t appear in everyone. Flu-like symptoms and fatigue are other noticeable signs of infection.

Public Health England says the best way for walkers to avoid getting bitten is to use repellent, wear light coloured clothes so that ticks can easily be seen and walk on paths and avoid long grass or verges. Dog walkers are also advised to check their pets as ticks spread other diseases as well as Lyme disease to animals as well.

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For those worried about their gardens, keeping lawns short, raking up leaf litter and creating a buffer zone between habitats ticks tend to like and lawn-paving, wood chips and gravel can help.

However, Prof Wall says a very small proportion of ticks carry Lyme disease.

Who, what, why?

A part of BBC News Magazine, Who, What, Why? aims to answer questions behind the headlines

Dr Brooks says the disease is a far bigger problem in other parts of Europe and the US, especially on the East Coast.

The most important thing is for those that think they might have symptoms of Lyme disease to go to the GP as prompt treatment will prevent complications. Symptoms usually take between three days to six weeks to appear after a tick bite.

And for those unsure how to remove a tick? Use fine tipped tweezers, or a tick-removal tool, to grasp the tick by the head as close to the skin as possible. Pull firmly and steadily, without twisting, as this could increase the risk of infection by prompting the tick to regurgitate saliva into the bite wound.

After the tick is removed, apply antiseptic and beware of a rash.

www.bbc.co.uk

Frontiers in Cellular
and Infection Microbiology

Parasite and Host

Edited by
Brice ROTUREAU

Institut Pasteur, France

Reviewed by
Guido Favia

University of Camerino, Italy

Emiliano Mori

Department of Life Sciences, University of Siena, Italy

Dana K. Shaw

Washington State University, United States

The editor and reviewers’ affiliations are the latest provided on their Loop research profiles and may not reflect their situation at the time of review.

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Review ARTICLE

Human Tick-Borne Diseases in Australia

  • 1 Neuroinflammation Group, Faculty of Medicine and Health Sciences, Macquarie University, Sydney, NSW, Australia
  • 2 Department of Microbial Biotechnology, School of Biology and Centre of Excellence in Phylogeny of Living Organisms, College of Science, University of Tehran, Tehran, Iran
  • 3 Charles Perkins Centre, School of Life and Environmental Sciences and Sydney Medical School, Marie Bashir Institute for Infectious Diseases and Biosecurity, The University of Sydney, Sydney, NSW, Australia
  • 4 Department of Microbiology and Infectious Disease, Royal North Shore Hospital, Sydney, NSW, Australia
  • 5 Grove Health Centre, Gordon, NSW, Australia

There are 17 human-biting ticks known in Australia. The bites of Ixodes holocyclus, Ornithodoros capensis, and Ornithodoros gurneyi can cause paralysis, inflammation, and severe local and systemic reactions in humans, respectively. Six ticks, including Amblyomma triguttatum, Bothriocroton hydrosauri, Haemaphysalis novaeguineae, Ixodes cornuatus, Ixodes holocyclus, and Ixodes tasmani may transmit Coxiella burnetii, Rickettsia australis, Rickettsia honei, or Rickettsia honei subsp. marmionii. These bacterial pathogens cause Q fever, Queensland tick typhus (QTT), Flinders Island spotted fever (FISF), and Australian spotted fever (ASF). It is also believed that babesiosis can be transmitted by ticks to humans in Australia. In addition, Argas robertsi, Haemaphysalis bancrofti, Haemaphysalis longicornis, Ixodes hirsti, Rhipicephalus australis, and Rhipicephalus sanguineus ticks may play active roles in transmission of other pathogens that already exist or could potentially be introduced into Australia. These pathogens include Anaplasma spp., Bartonella spp., Burkholderia spp., Francisella spp., Dera Ghazi Khan virus (DGKV), tick-borne encephalitis virus (TBEV), Lake Clarendon virus (LCV), Saumarez Reef virus (SREV), Upolu virus (UPOV), or Vinegar Hill virus (VINHV). It is important to regularly update clinicians’ knowledge about tick-borne infections because these bacteria and arboviruses are pathogens of humans that may cause fatal illness. An increase in the incidence of tick-borne infections of human may be observed in the future due to changes in demography, climate change, and increase in travel and shipments and even migratory patterns of birds or other animals. Moreover, the geographical conditions of Australia are favorable for many exotic ticks, which may become endemic to Australia given an opportunity. There are some human pathogens, such as Rickettsia conorii and Rickettsia rickettsii that are not currently present in Australia, but can be transmitted by some human-biting ticks found in Australia, such as Rhipicephalus sanguineus, if they enter and establish in this country. Despite these threats, our knowledge of Australian ticks and tick-borne diseases is in its infancy.

Background

Ticks and mosquitoes are recognized as the most important vectors in the transmission of bacterial and viral pathogens to humans and animals worldwide (Colwell et al., 2011). Ticks show marked genetic diversity with numerous species being mainly found in three families, viz. Argasidae, Ixodidae, and Nuttalliellidae. They can feed on various hosts and transmit or receive pathogenic bacteria, helminths, protozoa, and viruses to/from their host animals and humans. Although most studies have found that ticks and tick-borne illnesses are often limited to specific geographical regions, they may potentially be found anywhere in the world. International travel from endemic regions to non-endemic regions by people, animals and cargo can transport ticks. Whilst tick bites in Australia potentially can cause various diseases including bacterial and viral infections, paralysis, allergies, autoimmune disorders, post-infection fatigue and allegedly poorly quantified illnesses, the exact incidence of tick-borne disease in Australia is unknown (Graves and Stenos, 2017). Characterization of tick biology, tick-borne infections, and the distribution of ticks and tick-borne diseases can provide knowledge on their biological processes including tick immunity, reproduction, salivation, as well as tick-borne pathogens. This information is crucial for developing innovative strategies to control ticks and tick-borne disease. Understanding the microorganisms-host relationship could be exploited for our benefits (Dehhaghi et al., 2018). In case of tick-borne pathogens, such knowledge could be used for developing preventive mechanisms either for establishment of pathogens or their transmission. In this review, we will examine the geographical distribution of human-biting ticks in Australia, the reported tick-borne diseases, and potential of these ticks to carry emerging pathogens of humans and their possible transmission to humans. Allergic manifestations of tick bite are potentially life-threatening and not uncommon but are outside the scope of this paper.

Australian Ticks

There are 896 valid species of ticks worldwide, distributed in two main families of Argasidae (soft ticks) and Ixodidae (hard ticks) (Guglielmone et al., 2010; Barker et al., 2014). The major proposed events in the evolution of ticks are shown in Figure 1 (Klompen et al., 1996; Dobson and Barker, 1999; Murrell et al., 2001; Mans et al., 2012; Barker et al., 2014). Australia has unique climatic and environmental conditions that are favorable for six of the eight subfamilies of ticks including Amblyomminae, Argasinae, Bothriocrotinae, Haemaphysalinae, Ixodinae, and Ornithodorinae. Despite this faunal richness, only

8% of all valid tick species are endemic to Australia, comprising 14 soft ticks and 58 hard ticks, mainly feeding on wildlife (Barker et al., 2014; Ash et al., 2017; Kwak et al., 2018). Of these, 17 species may attach and feed on humans and domestic animals (Table 1), whereas the remaining 55 ticks mainly feed on birds, wild reptiles, and wild mammals.

Figure 1. Major events in tick evolution.

Table 1. Human-biting ticks of Australia with their habitats and main hosts.

The overall aim of this review is to provide relevant information on tick-borne diseases in humans; as such, only those ticks which been proven as vectors of human pathogens are discussed. The classification of 17 human-biting ticks is shown in Figure 2. Amongst them, Argas persicus, Haemaphysalis longicornis, Otobius megnini, Rhipicephalus australis, and Rhipicephalus sanguineus have been accidentally introduced into Australia by humans (Barker et al., 2014).

Figure 2. Classification of Australian human-biting ticks. Tick-borne diseases of humans that are transmitted (red boxes with vertical lines), potential tick-borne diseases of humans that may be transmitted (yellow boxes with dots), and other human-biting ticks (white boxes with upward diagonals).

Ornithodoros capensis, previously known as Carios capensis, feeds primarily on seabirds, although it can bite humans if the opportunity is provided. Off-shore islands are the most likely place that this tick bites humans because they provide nesting grounds for seabirds; therefore, campers, explorers, and those who participate in recreational and professional fishing are at higher risk. Ornithodoros gurneyi is exclusively a desert-dwelling tick in Australia that lives mainly in the wallows of desert-dwelling kangaroos and hence rarely encounters livestock or humans. However, this tick quests in soil and ambushes humans and other mammals if they rest under a desert-tree or in a desert-cave. The bites of O. capensis and O. gurneyi cause inflammation and severe local and systemic reactions in humans, respectively. In addition, a bite from the former tick species may cause blistering, dull ache, erythema, general lassitude and discomfort, intense pruritus, lesions, lymphangitis, rheumatic pain, and weeping; whereas the latter may cause headache, impaired vision, temporary blindness, swelling, and vomiting (Henary, 1938; Barker and Walker, 2014). O. megnini is eyeless and may feed on people who are in close contact with horses. There are no reports of transmission of any pathogens by this tick to its hosts. However, tick spines as well as feeding in the ear canal causes considerable irritation, inflammation, and tissue necrosis of the ear which may lead to bacterial infections.

Of the 18 valid species of Amblyomma in Australia, only Amblyomma triguttatum is regularly reported on domestic animals and has been taken from humans (Barker and Walker, 2014). Bothriocroton auruginans is a tick with an unknown life-cycle but its larvae and nymphs may attack domestic dogs without developing any illness. However, the adult tick is strictly host specific and to date its adult form has been only found on wombats (Barker and Walker, 2014). Bothriocroton hydrosauri, previously known as Aponomma hydrosauri, is one of the most commonly studied ticks in Australia. It feeds on reptiles in southern Australia as well as cattle, horses and humans. For many years, it was believed that H. longicornis is a possible vector of Theileria orientalis in New South Wales. However, despite the reports of its ability to transmit some bacteria and viruses in other parts of the world, it is not a known vector of any pathogens in Australia or has limited vectorial capacity of T. orientalis (Stewart et al., 1996; Barker and Walker, 2014).

Ixodes cornuatus, Ixodes hirsti, and Ixodes holocyclus can cause paralysis in their hosts. In Tasmania, I. cornuatus is the only tick that has been clinically associated with paralysis and is the most common tick found on domestic animals. In contrast, I. holocyclus is the most common tick that causes tick paralysis in domestic animals, humans, and wildlife in Australia. Although I. holocyclus feeds on various birds and mammals, it needs bandicoots to sustain its life cycle and population (Barker and Walker, 2014). Ixodes tasmani has the most widespread geographic distribution as well as the broadest range of hosts of any Australian tick. These three species of Ixodes ticks occur only in Australia, with the exception of I. cornuatus which is also found in Papua New Guinea (Arundel, 1988; Barker and Walker, 2014). R. australis, previously known as Boophilus microplus, primarily feeds on cattle, but its larvae and young adults, especially males, may feed on humans. However, the tick is usually removed by a human host due to local irritation and itching. There is a reported case (Green, 1971) of a female R. australis producing viable eggs following attachment to and feeding on a human host. R. sanguineus is the most widespread tick in tropical and sub-tropical areas of Australia owing to its specialized feeding on domestic dogs, which are its hosts for all life stages (Barker and Walker, 2014). When dogs are not available, this tick seeks other hosts such as cattle to maintain tick populations. Additionally, the immature forms of this tick may attach to humans. This tick species can carry different human health-threatening pathogens. Some of these pathogens include Rickettsia cornii, the cause of “boutonneuse fever,” and Rickettsia rickettsii, the cause of Brazilian spotted fever and Rocky Mountain spotted fever, are not present in Australia yet.

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In Australia, only six out of 17 human-biting ticks act as competent vectors for the transmission of pathogens to humans. They include A. triguttatum, B. hydrosauri, Haemaphysalis novaeguineae, I. cornuatus, I. holocyclus, and I. tasmani (Barker and Walker, 2014). Figure 3 shows the geographical distribution of those six competent ticks and an additional four ticks that carry or have potential to carry human pathogens as well as the distribution of tick-borne infections of humans in Australia. It is important to note in this context that the ability to carry pathogens is different from the ability to transmit them, and active transmission has yet to be established in some cases. New South Wales, Queensland, Tasmania, Victoria, and Western Australia are endemic to at least one tick-borne infection of humans. In contrast, no tick-borne infections of humans are known to occur in north, west, and south-west portions of South Australia as well as the Northern Territory States. Significantly, the tick fauna of all states in Australia have potential to transmit new and emerging pathogens of humans. The only exceptions may be some areas within Northern Territory and South Australia States. It is unclear why no human-biting tick or tick-borne human infection has been reported from these areas. It may be because of tick density or simply lower number of field examinations. The sustainability of tick-borne pathogens within a specific geographical location is determined by tick population density, which itself is controlled by hosts population densities and tick mortality rates. The biotic (predation) and abiotic (climate including desiccation, drowning, extreme temperature) characteristics of any one location influence the host density. Moreover, environmental factors are a determinant for mortality rates of free-living tick; therefore, the suitability of specific habitat for tick population invasion, establishment, and persistence is important. For instance, larvae of I. holocyclus and, to lesser extent, its engorged nymphs are highly susceptible to desiccation which confines them to a narrow coastal strip with low temperatures, high humidity, and existence of hosts. It is important to emphasize that climatic patterns have direct influence on tick survival rates as mentioned earlier; critically, therefore, climate change may occasionally or permanently provide particularly favorable conditions for tick survival, increasing tick densities and exposing more humans to tick-borne pathogens. Hence, the epidemiology of ticks and tick-borne pathogens of humans also must be studied in respect to climate change and ecology. It should be also noted that any variation in fauna could change the transmission risk for tick-borne diseases through addition of new reservoir and/or amplification of the circulation of native or exotic pathogens (Marsot et al., 2013).

Figure 3. Geographical distribution of 10 potentially human biting-ticks of Australia; Tick-borne diseases of humans that are transmitted (red and 1) and potential tick-borne diseases of humans that may be transmitted (yellow and 2).

Bacterial Tick-Borne Infections

Q fever and some rickettsial infections (see section -Q fever and Rickettsial infections) are the only bacterial diseases that are believed to be transmitted by human-biting ticks in Australia. However, ticks that bite humans may also be potential vectors for transmitting human pathogens that cause anaplasmosis, bartonellosis, Lyme-like disease, melioidosis, and tularemia in this country. The phylogenetic analysis of the causative pathogens of these diseases is shown in Figure 4.

Figure 4. Phylogenetic analysis of pathogenic bacteria of humans that are transmitted (red and *) or could potentially be transmitted by human-biting ticks (black) in Australia inferred using a Maximum Likelihood method based on the 16S rRNA gene sequence comparison (1,400 to 1,500 nucleotides).

Q Fever

Coxiella is a genus of bacteria of the family Coxiellaceae, order Legionellales, class Gammaproteobacteria, and phylum Proteobacteria. Coxiella burnetii is the causative agent of Q fever. It was previously classified as a Rickettsia species due to morphological similarities. However, it has now been placed into the gamma subdivision of Proteobacteria based on genetic and physiologic characteristics, with closer similarities to Legionella and Francisella than to Rickettsia (Roest et al., 2013). This obligate intracellular Gram-negative bacterium protects itself in hostile environments by forming spores which can survive for long periods, for example 586 days in tick feces at room temperature (Philip, 1948). In mammals, macrophages are unable to kill Coxiella burnetii and the pathogen may persist asymptomatically. Furthermore, C. burnetii demonstrates antigenic shift, a phenomenon that is the basis of serology tests used to differentiate acute from chronic Q fever (Million et al., 2010).

Q fever notification rates decreased over 50% from 2002 to 2005, following the introduction of a nationally funded Q fever vaccination program in Australia (Gidding et al., 2009). However, this vaccine has significant side effects in persons exposed to C. burnetii and therefore requires pre-vaccination screening (Madariaga et al., 2003; Gidding et al., 2009). This pathogen affects a large variety of domestic (e.g., cattle, cats, goats, sheep) and wild animals as well as humans. According to Australian government Department of Health, the incidence rate of Q fever in Australia in 2005 was 17.2 per each million of the population. Currently, this disease is the most reported zoonosis in Australia. However, it should be noted that many people suffering from Q fever remain asymptomatic or only show a self-limiting febrile illness and hence are not included in calculations of incidence rate. The geographical distribution of Q fever includes Queensland and northeast New South Wales; however, it is emerging in other regions, for examples, Northern Territory and southwest Western Australia (Gidding et al., 2009).

More than 40 species of ticks can carry C. burnetii worldwide; there is, however, controversy over their importance in epidemiology of Q fever (Duron et al., 2015) because inhalation of infectious aerosols or dust particles remains the main route of the disease transmission. Ticks, including Haemaphysalis bispinosa, Haemaphysalis humerosa, I. holocyclus, Rhipicephalus microplus, and R. sanguineus may have roles in Q fever epidemiology in Australia (Smith, 1941). Accordingly, H. humerosa and I. holocyclus are competent vectors for C. burnetii and can acquire the pathogen from an infected animal and transmit it to an uninfected animal, but for the other three ticks not enough information is available to assess the vector competency for this pathogen (Smith, 1941).

The pathogen is vertically transmitted trans-stadailly from larva to nymph and from nymph to adult in the abovementioned ticks, with the exception of H. bispinosa and R. microplus. H. bispinosa show trans-stadial transmission only from larva to nymph (Duron et al., 2015). No information has been provided on the ability of H. bispinosa and R. sanguineus to transmit C. burnetii to animals. However, studies showed that I. holocyclus and R. microplus could only transmit infection from these ticks to guinea pigs by feces and bite, respectively. Despite the demonstrated transmission of C. burnetii in experimental systems, ticks only occasionally transmit the pathogen in the field (Duron et al., 2015). No solid information is available on tick-borne Q fever in Australian populations. Occasional case reports only suggest the possibility. For example, a human case of acute Q fever with pericarditis north-east of Perth in Western Australia has been described (Beaman and Hung, 1989) as transmitted directly by A. triguttatum bite. Symptoms may include abdominal and thoracic pain, bradycardia, chills, headache, high fever, myalgia, and pharyngitis after a 2–4-week incubation period. Compared to rickettsial infections, Q fever is unlikely to be associated with a rash. Apparent lung involvement may be absent as many cases present with fever, with no localizing signs, although hepatitis is common. Q fever is typically diagnosed by serology but can also be confirmed by more specialized, albeit less accessible, tests such as immunohistochemistry and polymerase chain reaction (PCR). Isolation of C. burnetii can only be performed in biosafety three (BSL-3) facilities, owing to its high infectivity.

Rickettsial Infections

Rickettsia is a genus of non-motile, non-spore forming, obligate intracellular, Gram-negative bacteria that belongs to family Rickettsiaceae, order Rickettsiales, class Alphaproteobacteria, phylum Proteobacteria. Rickettsia obtains energy by parasitising vascular endothelial cells and macrophages in mammalian target organs. This pathogen can be transmitted vertically between invertebrates through life stages or be transmitted horizontally from invertebrates to vertebrates or vice versa during feeding of the tick on its host (Weinert et al., 2009). It is serologically categorized into two major classes, namely, the spotted fever group (SFG) and the typhus group. SFG rickettsia has two new sister groups: the ancestral group (AG), and the transitional group (TRG). All the members in SFG and AG, as well as Rickettsia australis from TRG are transmitted by tick and together these organisms encompass more than 36 tick-borne species. Of these, 15 species have been implicated as causal agents for a variety of human illnesses.

In Australia, three species including R. australis, Rickettsia honei (including its novel strain Rickettsia honei marmionii), and Rickettsia gravesii can be transmitted by bite of one or more ticks species, including A. triguttatum B. hydrosauri, H. novaeguineae, I. cornuatus, I. holocyclus, and I. tasmani. Unfortunately, no incidence rate has been reported for rickettsial diseases in Australia, but the annual rate of SFG rickettsioses surged up to 8.5 folds from 2008 to 2012, reaching 14.3 cases per each million populations (Drexler et al., 2016). The symptoms of these infections include eschar, fatigue, fever, headache, myalgia, and rash (macular, popular, vesicular). They are typically seen in residents of endemic areas as well as campers, travelers, and hikers to endemic areas. The severity and duration of rickettsial diseases vary considerably. Table 2 presents some information on different SFG rickettsial diseases in Australia.

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Table 2. Spotted fever group rickettsia in Australia.

The genetic variation in Australian SFG rickettsia has been classified into two populations (Baird et al., 1996). R. australis and R. honei were designated as etiological agents of Queensland tick typhus (QTT) and Flinders Island spotted fever (FISF), respectively. Furthermore, R. honei strain marmionii causes Australian spotted fever (ASF). Whilst, ASF, FISF and QTT diseases have similar clinical and serological characteristics, their causative pathogens have varying plaque-forming abilities on different culture media. Additionally, characterization of the gene responsible for encoding the genus-specific 17-kDa antigen of R. australis revealed a distinct nucleotide sequence, compared to those of R. honei (Baird et al., 1992).

Southern blot analysis of isolates from patients with FISF and QTT showed clear differences in banding patterns when a probe for the rRNA genes is used (Baird et al., 1992). Both species respond well to antibiotic therapy with doxycycline. A new possible class of Australian SFG rickettsia has been recently proposed, following reports of possible rickettsiosis among local workers (Owen et al., 2006; Sentausa et al., 2013; Abdad et al., 2017). According to these studies, R. gravesii can use A. triguttatum as a vector to infect humans. This tick-borne disease has been reported on Barrow Island in the north-west coast of Western Australia.

Although it is also found in Amblyomma limbatum, no confirmed report of transmission of R. gravesii by this tick has been published yet. QTT is an emerging public health threat along the whole eastern seaboard of Australia. Cases may occur throughout the year. The geographical distribution of the aetiologic agent, R. australis, is expanding due to changes in climate and human population demographics (Stewart et al., 2017). I. cornuatus, I. holocyclus, and I. tasmani have been identified as the main vectors of this pathogen. The first description of QTT was reported from Queensland in 1946 with subsequent similar cases reported in New South Wales and Victoria (Pinn and Sowden, 1998). Generally, QTT is considered as relatively mild illness with symptoms of enlarged lymph nodes, fever, headache, maculopapular or vesicular rash, and malaise. Other possible symptoms include chills, cough, eschar, and myalgia. In 1991, a study reported the incident of SFG rickettsial infections in East Gippsland in Victoria with no identification of the causative Rickettsia sp. (Dwyer et al., 1991). In the same year, information on 62 Australian cases of SFG rickettsial infections from New South Wales, Queensland, and Victoria were also reviewed (Sexton et al., 1991). This included a fatal case of a healthy 68-year-old male from Mossman in Queensland (Sexton et al., 1990). The authors concluded that R. australis was the causative agent of all cases.

In 2007, three suspected cases of QTT were reported. Each case displayed complications including renal failure and severe pneumonia (McBride et al., 2007). More recently, five cases of QTT were reported from southern coastal New South Wales (Fergie et al., 2017), in which illness was characterized by a cutaneous eruption of erythematous papules and pustules as well as lymphadenopathy. Acute delirium or acute kidney injury was observed in three of the five cases. Improved awareness of the condition and its complications amongst the community and its clinicians is imperative to enable early diagnosis and treatment.

R. honei is the etiological agent of FISF (Stenos et al., 1998) and is transmitted by B. hydrosauri. FISF was first described on Flinders Island in Tasmania in 1991 and the causative organism was characterized (Graves et al., 1991). Symptoms include cough, fever, headache, maculopapular rash, myalgia, and transient arthralgia. FISF was initially thought to be restricted to south-eastern Australia with highest prevalence in summer, but new cases from previously non-endemic areas for this infection, including south-western coastal areas of Western Australia in Salisbury Island and Walpole, and south-eastern coastal regions of South Australia near Adelaide have been reported (Graves et al., 1991, 1993; Dyer et al., 2005; Unsworth et al., 2007).

In 2007, seven cases of SFG rickettsial diseases similar to FISF were reported from eastern Australia (Unsworth et al., 2007). Genetic identification of the etiologic agent of the disease showed close genetic relationship to R. honei, with also low similarities to R. australis. Therefore, a new strain of Rickettsia, R. honei subsp. marmionii, was designated as the causative agent of the rickettsiosis (Unsworth et al., 2007). To distinguish infection caused by R. honei marmionii from that of caused by R. honei, the name ASF was adopted. Unfortunately, no information is available on the epidemiology and ecology of its tick vector, H. novaeguineae, within Australia yet.

Potential Bacterial Tick-Borne Infections

Several pathogenic bacteria have been isolated from human-biting ticks collected within Australia or have been transmitted in other parts of the globe by ticks of genera endemic in Australia. Some of these diseases, including anaplasmosis, bartonellosis, melioidosis, and tularemia have been discussed in this review. The incident rates of each of these potential disease has been provided in respect to Australia (if available) or other regions in the world to provide the readers a clue about their potential public health risks.

Anaplasmosis

Human granulocytic anaplasmosis (HGA), formerly known as human granulocytic ehrlichiosis, is an acute febrile disease caused by the rickettsial bacterium Anaplasma phagocytophilum, previously known as Ehrlichia phagocytophilum. This pathogen is transmitted by ticks, particularly the genera Amblyomma, Dermacentor, Ixodes, and Rhipicephalus. A. phagocytophilum is an obligate intracellular, Gram-negative bacterium in family Ehrlichiaceae, order Rickettsiales, class Alphaproteobacteria, and phylum Proteobacteria. This pathogen infects granulocytes and survives by suppressing or postponing vital antimicrobial mechanisms including apoptosis, oxidative burst, and phagocytosis as well as by reducing expression of defense genes in host cells. The clinical presentation is an acute, febrile, non-specific, viral-like disease with common early symptoms of headache, elevated hepatic transaminase, leukopaenia, myalgias, and thrombocytopaenia.

The incidence of HGA (cases/million/year) jumped from 1.4 in 2000 to 6.1 in 2010 and 6.3 in 2012. Although, there are as yet no reports of HGA in Australia, data is limited. Bacterial profiling of 460 ticks from four Australian human-biting tick species, namely, A. triguttatum, Haemaphysalis bancrofti, H. longicornis, and I. holocyclus were recently conducted (Gofton et al., 2015a). A novel Anaplasma sp. was identified in about 2% of A. triguttatum ticks. Other studies draw attention to the competence of R. sanguineus and R. australis in transmission of Anaplasma spp. (Bock et al., 1999; Rymaszewska and Grenda, 2008), both of which are also found in Australia. Further investigation is required to determine whether these ticks or other ticks within Australia can act as a vector for A. phagocytophilum and subsequently transmit Anaplasma to humans or not.

Bartonellosis

Bartonella is a genus of facultative intracellular, Gram-negative bacteria belonging to family Bartonellaceae, order Rhizobiales, class Alphaproteobacteria, phylum Proteobacteria. The three most common human diseases caused by this genus are Carrion’s disease, cat scratch disease, and trench fever. The pathogenic agents of these diseases are Bartonella bacilliformis, Bartonella henselae, and Bartonella quintana, respectively. The only information about incidence of bartonellosis belongs to cat scratch disease in United States (94 cases/million people) between 2005 and 2013 (Nelson et al., 2016). These diseases are transmitted when humans are scratched by domestic or feral cats or by contact with arthropods including body louse, fleas, or sand flies. Symptoms and signs include a papule or pustule at the inoculation site, abdominal pain, bacillary angiomatosis (lesions in the skin, subcutaneous tissue, bone, or other organs), bacillary peliosis (vascular lesions in liver and spleen), bone pain, fever, enlarged lymph nodes, headache, rash, severe anemia, and subacute endocarditis. In Australia, Bartonella clarridgeiae and Bartonella henselae are found in cats, cat fleas and humans. Bartonella henselae sequence type 1 or strain Houston-1 is believed to be the major etiological agent of human bartonellosis and is distributed in up to 35% of the younger than 1-year cat population of Australia (Iredell et al., 2003; Arvand et al., 2007; Barrs et al., 2010; Kaewmongkol et al., 2011a). Additionally, novel Bartonella spp. have been identified in mammalian hosts in Australia. These include Bartonella australis, Bartonella coopersplainsensis, Bartonella queenslandensis, Bartonella rattaustraliani, Candidatus Bartonella antechini, isolated from eastern gray kangaroos (Macropus giganteus), Uromys spp., Melomys spp., Rattus spp., and mardo or yellow-footed antechinus (Antechinus flavipes), respectively (Dehio, 2008; Gundi et al., 2009; Kaewmongkol et al., 2011b).

At least eight Bartonella spp. are carried by some ticks within Australia, viz. Bartonella rattaustraliani by Ixodes spp., Candidatus Bartonella antechini n. sp. by Ixodes antechini, Candidatus Bartonella woyliei n. sp. by Ixodes australiensis, and five uncultured and unpublished Bartonella spp. (genotypes accession numbers EF662053 to EF662057) by perhaps I. tasmani (Vilcins et al., 2009; Kaewmongkol et al., 2011a). These ticks were collected from various animals, including koalas (Phascolarctos cinereus), rodents, woylies (Bettongia penicillata), or yellow-footed antechinus (Antechinus flavipes). Despite these findings, there is currently no convincing evidence that verifies tick-borne transmission of Bartonella infection to humans, in Australia. However, this possibility should not be excluded until tick-borne bartonellosis is either rejected or accepted by the performance of well-conducted, detailed studies of the relationship between humans, ticks and tick-associated Bartonella species (CDC, 2015).

Lyme and Lyme-Like Diseases

Lyme disease (or lyme borreliosis) is another tick-borne disease caused by genus Borrelia in family Spirochaetaceae, order Spirochaetales, and phylum Spirochates (Paster and Dewhirst, 2000) This spirochete is generally transmitted by Ixodes ticks with life-cycles that involve birds and non-human mammalian hosts (Chalada et al., 2016). The annual incidence rates of Lyme disease in England and Wales are Keywords: anaplasmosis, arbovirus, babesiosis, bartonellosis, Lyme-like disease, Q fever, rickettsial infection, tick paralysis

Citation: Dehhaghi M, Kazemi Shariat Panahi H, Holmes EC, Hudson BJ, Schloeffel R and Guillemin GJ (2019) Human Tick-Borne Diseases in Australia. Front. Cell. Infect. Microbiol. 9:3. doi: 10.3389/fcimb.2019.00003

Received: 27 November 2018; Accepted: 07 January 2019;
Published: 28 January 2019.

Brice Rotureau, Institut Pasteur, France

Emiliano Mori, Università degli Studi di Siena, Italy
Guido Favia, University of Camerino, Italy
Dana Kathleen Shaw, Washington State University, United States

Copyright © 2019 Dehhaghi, Kazemi Shariat Panahi, Holmes, Hudson, Schloeffel and Guillemin. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

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