Talk:Feral pigeon/Archive 2
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Health risks ambiguity, whose immune system?
Under the section ‘Potential health risks to humans’ the second sentence states “However, it is rare that a pigeon will transmit a disease to humans due to their immune system.” Whose immune system? I assume humans' is meant and it seems the more likely but it could conceivably refer to the pigeons' (isn't it possible that the pigeons' immune system renders the pathogen harmless?). I admit I didn't read the reference (21 – I might yet do that and will edit this comment accordingly if I do) but its title doesn't clarify matters: it's a PDF entitled ‘Public health significance of urban pests’. I guess only the author is really qualified to edit as they're the only person who knows which they meant, unless anyone's knowledgeable enough to know categorically that it can't be a pigeon's? If it is the human immune system, changing ‘their’ to ‘our’ would suffice to clear up the ambiguity. If it is the pigeons', something like “However, due to a pigeon's immune system it is rare that they will transmit a disease to humans.” Should anyone think it worth editing the article to remove this ambiguity of course you aren't obliged to adhere to my suggestions. I only made them as they're the most minimal I could think of (my first inclination was to change the sentence to “However, due to their immune system it is rare that pigeons will transmit a disease to humans.” but I realized that, while less obviously so – it would be a rather unusual and clumsy construction if the human immune system was meant –, it's actually still ambiguous). If the intention of an edit is to remove an ambiguity then surely it's best not to replace it with a lesser one? SaintIX (talk) 17:16, 23 June 2024 (UTC)
- Fair question. Find below a wikitextual copy of of the relevant sections of that reference, with handy-dandy highlighting. It should be slightly easier to figure out what the original statement was supposed to mean, if it was not synthesis or in some other way inaccurately interpreted. There's a significant amount of information (though large parts are kept purely for context and contain no directly relevant info), and the statement might be expanded or completely removed or replaced if found to be unsupported or a work of fiction. I'll have a deeper read myself in the coming days, but am very tired right now.
- Minor errors may exist since the reformatting required was horrible, so check against the original before nailing anything down.
Fred Gandt · talk · contribs02:29, 25 June 2024 (UTC)- @Fred Gandt Thank you, that's very kind of you and I'm sure it'll be considerably easier than reading the article. I have actually downloaded the PDF (‘Public significance of urban pests’) but haven't got round to reading it yet. I was unable to access ‘Health hazards posed by feral pigeons’ in full (ref #22), as it requires a subscription via an institution or could be bought from the Journal of Infection (subscriptions to scientific/academic journals tend to be quite pricey¹. I could only read the summary and part of the first paragraph of various sections of the article. However, I gleaned enough information to conclude that the paragraph was composed from a mix of the two references (based on the fact that the figure five for the commonly transmitted pathogens came from ref #21, not #22 (which gives it as seven). Anyway, thanks again for your kind help and I wish you a speedy recovery from your fatigue.
- ¹ This footnote is about journal subscriptions: I liked into accessing options for the article I couldn't access. It took a fair while and some effort so I thought I'd share my findings, in case anyone's interested but feel free to skip these paragraphs if not. They are quite long but that's why I've included them as a footnote, so you can skip them if you're not interested. It's only indirectly relevant to the subject under discussion, insofar as anyone's considering a subscription for research purposes. Given the cost I would think most people would forget the idea unless they have a genuine interest in the subject anyway.
- Subscriptions to scientific journals tend to be pretty expensive (I used to work at the Royal Society of Medicine (RSM) library which subscribed to all but the most obscure English language medical journals and the budget for that was in the £100,000s per year!): a PDF of this article for reasearch/personal use is $27.95. Most books don't cost that much, this is just one article! For corporations it's $37.95, and clinicians can access it via a free 15-day trial of ‘ClinicalKey’ (an Elsevier app that gives you access to articles from a selection of Elsevier scientific journals (but not in the essentials package; qv below), books and a few other resources like lectures, videos &c. However, I was curious how much a subscription would cost as I'm always suspicious of ‘free’ trials. I've fallen foul of cancelling subscriptions in time on a couple of occasions (despite setting reminders 1 day before and on the day due at 12:00, 18:00 & 21:00) and I'm sure that part of the strategy behind these offers is profitting from such mistakes. I don't like giving my debit card details unless I'm actually buying something and the fact that they always ask for one is proof enough for me that they're definitely hoping for these kind of oversights, otherwise they wouldn't ask for your details until the trial expires or at least warn you it's about to expire and you need to cancel within the relevant period if you don't want to continue. I've never come across a trial where they do that. Other sneaky practices are small print conditions that say you have to cancel at least 24-48 hours before your payment is due (that's the one that caught me out). Anyway…
- The ClinicalKey website doesn't mention a price, it just takes you to a ‘contact us’ page with a lengthy form to fill in (name, address, email, phone, institute, institute email, institute phone, specialty… it went on and on. A general search for subscription prices did result produce a link (so why didn't the company's website's search feature show that page? My guess is that they want you to actually talk to them so they can apply sales pressure and techniques) which showed three prices/price ranges: essentials package $299/year or $29/month: gives access to abstracts, books, videos & lectures; specialty package $500-$750/year or $60-$125/month: essentials plus access to journals and clinics for the chosen specialty and extended specialty package $1,040-$1,250/year or $125-$200/month: gives access for up to six specialties' journals & clinics! Ouch 😳 🤕! On the other hand, considering that many journals cost over $100 per year (for example, Nature is 202.72€ per year, roughly $215), those rates don't seem so bad but it does make the $28 look reasonable. If you only access 10 articles or fewer a year (and assuming this is an average price), you'd be better of buying the articles individually. I did warn you it was pricey. It's pretty much unaffordable to a lay person or someone researching for Wikipedia articles. I guess the authors of those articles are either rich or work for an institute that allows them access. I don't think ordinary local libraries give that kind of access, although the British Library might (the RSM was one of 17 specialist backup libraries for the British Library. I was actually responsible for its BL Backup Department (actually, I WAS the BL Backup Department 🙂). You could ask for an interlibrary loan but they cost £10-£20 (roughly $12.50-$25 depending on whether they're inland or overseas, so £10 for this particular article. That's almost ⅓ of the price but it's still not cheap).
- SaintIX (talk) 20:19, 26 June 2024 (UTC)
- Check out the Wikipedia Library.
Fred Gandt · talk · contribs22:07, 26 June 2024 (UTC)
- Check out the Wikipedia Library.
The pigeon relevant sections of that .pdf reference for convenience
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Several figures and tables omitted 8. Birds Summary Beside the harm some wild urban bird species (mostly feral pigeons) cause to buildings by their activity and droppings, their nesting sites can be the source of abundant ectoparasites (such as argasid ticks, mites, bugs and fleas) that produce allergic reactions in people. Also, certain microorganisms pathogenic to people have been found to be associated with wild urban birds:
Cases of human disease acquired directly from urban birds or from their habitats have been reported for ornithosis, histoplasmosis, salmonellosis, campylobacterosis, mycobacteriosis, cryptococcosis, and toxoplasmosis. Monitoring zoonotic and sapronotic diseases associated with birds in urban areas is the first essential step in controlling these diseases. In circumstances of established risk, managing urban bird populations includes:
Also, proactive and reactive control measures can be implemented, such as:
This integrated management approach should also involve educational and legal components. 8.1. Introduction This chapter aims to review and assess the pertinent literature on wild birds in urban ecosystems – that is, birds that live in both urban and suburban habitats – and it includes the feral pigeon (Columba livia f. domestica) as a potential health hazard for people. The survey does not include wild birds kept in captivity (such as in zoological parks and aviaries), reared game, poultry and other domestic birds as a source of human infection, nor does it include pet birds in urban areas. The term synanthropic birds is sometimes used alternatively and means wild birds that live in association with people (in human habitats). 8.1.1. Free-living birds as so-called pests in the urban ecosystem Urban free-living birds could be called companion animals, especially for children, the elderly and lonely people: they are often watched or fed (or both) with pleasure by many city dwellers around the world who are deprived of the countryside (Fig. 8.1 and 8.2). These birds are usually considered to be an agreeable, pleasant component of the urban environment. In that sense, urban birds are not formidable pests. However, under some circumstances, some urban bird species (especially, pigeons, doves, gulls, house sparrows, starlings, blackbirds, grackles and corvids) that congregate at too high population densities produce droppings that harm such human artefacts as historical monuments, buildings, statues, fountains and cars (Fig. 8.3). Also, certain synanthropic avian species can be extremely noisy at feeding sites, breeding colonies and communal roosts (Fig. 8.4). Moreover, some of them can be harmful to urban vegetation (trees and such fruits as cherries) in gardens (blackbirds and starlings, for example) or cause additional pollution problems with their droppings, which foul yards, sidewalks (creating the risk of slipping and physical injury for pedestrians) and roads, and also produce foul odours. In so doing, such species as pigeons, gulls, starlings, grackles, blackbirds and corvids become a nuisance (Lesaffre, 1997; Odermatt et al., 1998). In addition, some medium-sized gregarious birds, such as gulls, rooks and lapwings, can cause dangerous aircraft accidents, during take-off and landing at suburban airfields. 8.1.2. Urban birds as a source of ectoparasites harmful to people In urban areas, nests of feral pigeons in the lofts of houses can result in invasions of soft ticks (such as the pigeon tick, Argas reflexus) into closely situated flats and apartments. Such invasions can result in infestations of their occupants (Dusbábek & Rosick´y, 1976) that often lead to allergic reactions (Glünder, 1989; Veraldi et al., 1998; Rolla et al., 2004). Other pigeon ectoparasites can occasionally attack humans as well. Examples of these are: mites, such as the chicken mite (Dermanyssus gallinae), which may produce allergic reactions, especially in children and susceptible adults; bugs, such as the pigeon bug (Cimex columbarius); and fleas, such as the pigeon flea (Ceratophyllus columbae) (Sixl, 1975; Glünder, 1989; Haag-Wackernagel, 2005). 8.1.3. Wild birds and human pathogenic microorganisms in general Yet another (and more serious) problem could arise: some urban birds are associated with microorganisms pathogenic to people; thus, these birds present a potential human health hazard. It is well established that wild birds, including those living in the urban ecosystem, can harbour pathogenic microorganisms and also spread them to people (Keymer, 1958; McDiarmid, 1969; Davis et al., 1971; Sixl, 1975; Lvov & Ilyichev, 1979; Glünder, 1989; Cooper, 1990; Glünder et al., 1991; Hubálek, 1994; Lesaffre, 1997; Wobeser, 1997; Haag-Wackernagel & Moch, 2004; Hubálek, 2004). In general, birds may be involved in the circulation of pathogenic microorganisms in a number of diverse ways:
From an epidemiological perspective, these infections can be regarded as either zoonoses (diseases transmitted from animals to people, as in cases 1–3) or sapronoses (diseases caused by organisms of the environment, as in case 4, where the causative agent requires a non-animal reservoir or site to replicate or complete the development) (Hubálek, 2003). 8.2. Human microbial pathogens associated with wild birds This section concisely reviews human microbial pathogens – viruses, bacteria, fungi and protozoa – that have been isolated from free-living birds in urban and suburban areas and from their haematophagous ectoparasites, excreta and nests. Omitted from consideration here are agents of avian diseases that usually do not cause clinical symptoms in people (such as Newcastle disease virus and other paramyxoviruses, avian circoviruses, avian coronaviruses, avian poxviruses, avian herpesviruses, Pasteurella multocida, avian trypanosomes, avian plasmodia, other avian haematozoa, and coccidiae), as well as microorganisms in whose circulation birds play a negligible role, compared with mammals (such as Venezuelan equine encephalitis virus and leptospirae). This section also assesses infections of people reported as attributable to, or directly associated with, urban birds. 8.2.1. Viruses 8.2.1.1. Togaviridae: genus Alphavirus 8.2.1.1.1. Eastern and Western equine encephalitis viruses In North America, birds are the principal hosts in the natural transmission of mosquitoborne Eastern and Western equine encephalitis viruses (EEEV and WEEV, respectively). These mosquito-borne viruses have also been isolated from synanthropic birds (mostly passerines and feral pigeons), but mainly during epidemics and epizootic episodes (Holden, 1955; Dardiri et al., 1957; Holden et al., 1973; Beran, 1981; Soler, Portales & Del Barrio, 1985). Some wild birds develop a relatively high-level, long-term viraemia after inoculation with WEEV and EEEV and can even maintain persistent virus infection, with viraemia lasting up to 10 months for WEEV (Hammon, Reeves & Sather, 1951; Kissling et al., 1954, 1957a,b; Reeves et al., 1958). Birds serve as a source of infectious blood to mosquito vectors and latently infected birds can be regarded as a virus reservoir. WEEV affects a wide range of wild birds, but it occurs less often than EEEV in epizootic episodes. For instance, mortality in Agelaius spp. blackbirds was observed after experimental infection with WEEV (Hardy, 1987). However, no EEEV or WEEV infections of people have been reported as attributable to, or directly associated with, urban birds. 8.2.1.1.2. Sindbis virus Birds are the principal hosts and disseminators of Sindbis virus (SINV; Scandinavian subtype: Ockelbo), while the vectors are largely ornithophilic mosquitoes. SINV was isolated from synanthropic species: carrion crows (Corvus corone) in Egypt (Taylor et al., 1955) and European starlings (Sturnus vulgaris) in Slovakia (Ernek et al., 1977). It causes encephalitis and occasional death in experimentally infected chickens and pigeons. The chronic course of the infection in pigeons has been ascertained experimentally (Semenov et al., 1973). However, no SINV infections of people have been reported as attributable to, or directly associated with, urban birds. 8.2.1.2. Flaviviridae: genus Flavivirus 8.2.1.2.1. St. Louis encephalitis virus Birds are principal amplifying hosts in endemic foci of St. Louis encephalitis virus (SLEV) in North and Central America (Theiler & Downs, 1973; Beran, 1981). House sparrows, feral pigeons and other synanthropic birds have often been used as sentinels for monitoring and predicting the epidemiological situation in urban areas (Holden et al., 1973; Lord et al., 1974; Lord, Calisher & Doughty, 1974; McLean et al., 1983). The house sparrow develops a relatively high-level, long-term viraemia (up to one month) and can serve as a source of infectious blood to mosquito vectors (Hammon, Reeves & Sather, 1951; Chamberlain et al., 1957). However, no SLEV infections of people have been reported as attributable to, or directly associated with, urban birds. 8.2.1.2.2. West Nile virus Birds are principal vertebrate hosts of this mosquito-borne agent. West Nile virus (WNV) was isolated from a number of synanthropic species – for example, feral pigeons and carrion crows in Egypt (Work, Hurlbut & Taylor, 1953; Hurlbut et al., 1956), black-headed gulls (Larus ridibundus) in Slovakia (Greˇsíková, Sekeyová & Prazniaková, 1975; Ernek et al., 1977), rooks (Corvus frugilegus) in Ukraine, carrion crows in the southern part of the European part of Russia, American crows (Corvus brachyrhynchos) in North America, and the common blackbird (Turdus merula) in Azerbaijan (Gaidamovich & Sokhey, 1973; Lvov & Ilyichev, 1979; Vinograd et al., 1982; Eidson et al., 2001). WNV sometimes causes a clinically manifest disease in feral pigeons and other free-living birds, with an occasional death (Hurlbut et al., 1956). Nevertheless, mass mortality of corvids (mostly American crows) and other birds has been observed during recent outbreaks of West Nile fever in North America, due to a high virulence of the virus strain for birds; the dying crows have therefore been used to monitor the epidemiological situation in urban areas of the United States (Eidson et al., 2001; Komar et al., 2003; Caffrey, Smith & Weston, 2005), and they probably contributed to the rapid east–west spread of WNV across North America since 2001. However, no WNV infections of people have been reported as attributable to, or directly associated with, urban birds. 8.2.1.2.3. Flaviviruses of the tick-borne encephalitis complex The principal hosts of tick-borne encephalitis (TBE) complex viruses are forest rodents, while birds are occasional hosts and disseminators of preimaginal (larval and nymphal stages of) ixodid ticks infected with TBE viruses. One of these viruses, the central European encephalitis virus (CEEV), was isolated occasionally from a few synanthropic birds – for example, the common blackbird and the song thrush (Turdus philomelos) in Finland (Brummer-Korvenkontio et al., 1973) and from common blackbirds and the great tit (Parus major) in the eastern Baltic region (Lvov & Ilyichev, 1979). Two CEEV strains were recovered from nymphal Ixodes ricinus (castor-bean) ticks collected on common blackbirds in Slovakia (Ernek et al., 1968). Most bird species are resistant to CEEV, including synanthropic house sparrows and great tits (Greˇsíková & Ernek, 1965); certain species, however, have been observed to develop viraemia that lasted several days after experimental infection with CEEV: common starling, song thrush, common blackbird (Saikku, 1973; Lvov & Ilyichev, 1979). Morbidity, mortality, and shedding of TBE viruses have been observed occasionally in experiments with the house sparrow (Lvov & Ilyichev, 1979). No human cases of TBE, however, have been reported as attributable to, or directly associated with, urban birds. 8.2.1.3. Orthomyxoviridae: genus Orthomyxovirus Influenza A virus has often been isolated from wild birds worldwide, mainly from ducks, gulls, terns, shearwaters and shorebirds, and less often from passerines (Lvov & Ilyichev, 1979; Wobeser, 1997; Lipkind, Shihmanter & Shoham, 1982; Hinshaw et al., 1985; Stallknecht & Shane, 1988; Webster et al., 1992; Munster et al., 2005), most strains being so-called low pathogenic avian influenza (LPAI) viruses. Wild aquatic birds are the primordial source and reservoir of all influenza viruses for other vertebrates (Hinshaw et al., 1981), and these birds perpetuate all known antigenic subtypes of influenza A viruses (H1–H16 and N1–N9). In wild ducks, influenza viruses replicate in the cells of the intestinal tract and are excreted in high concentrations in the faeces; the virus shedding can continue for 2–4 weeks (Slemons & Easterday, 1977; Hinshaw et al., 1980). Experimental infection of adult mallard ducks with the H5N2, H5N3 and H5N9 influenza A virus subtypes resulted in histologically demonstrated mild pneumonia, although clinical signs were not evident (Cooley et al., 1989). On the other hand, experimental infection of common starlings and house sparrows with an H7N7 influenza virus isolate from Australian chickens caused high mortality (100% in starlings and 30% in house sparrows) and transmission to contact birds, although it caused no mortality in ducks (Nestorowicz et al., 1987). In Italy, highly pathogenic avian influenza A (HPAI) strain H7N1 was isolated from two synanthropic birds (a house sparrow and a collared dove, Streptopelia decaocto) found dead, close to a chicken farm with an HPAI epizootic (Capua et al., 2000). In addition to HPAI viruses H5 and H7, LPAI strains circulate at a much higher frequency in such wild waterfowl as mallards (Anas platyrhynchos), and could convert to HPAI after being transmitted to poultry (Munster et al., 2005). South-east Asia is regarded as a region where influenza viruses co-circulate in urban and rural environments among people, domestic pigs and ducks, which provides the opportunity for interspecies transmission and genetic exchange among viruses (Webster et al., 1992). An extensive HPAI epornitic (an outbreak of disease in a bird population), caused by an H5N1 strain, started in domestic poultry in South-East Asia in 1997 and has raised special concern, because of its very rapid spread across Eurasia in 2005 and 2006 (Perdue & Swayne, 2005; WHO Global Influenza Program Surveillance Network, 2005). Some wild urban and suburban birds have also been involved – for example, feral pigeons and tree sparrows (Passer montanus) died from HPAI in China, Hong Kong SAR, Thailand and the Russian Federation (Ellis et al., 2004; Brown et al., 2005; FAO Avian Influenza Task Force, 2005; Morris & Jackson, 2005; N guyen et al., 2005). HPAI is mainly a veterinary (and economic) problem, and bird-to-human transmissions have been only sporadically reported: 271 human cases (165 of them fatal) have been confirmed in some countries in Asia and Africa but, as of 3 February 2007, no cases have been confirmed in Europe or North America (WHO, 2007). Obviously, people can become infected with HPAI only under very special circumstances: when they inhale or ingest a massive dose of virus, resulting from very intimate contact with infected domestic birds. Moreover, no human HPAI infection acquired from a wild bird has been described before April 2006. In brief, free-living urban birds do not present a risk of infecting people with HPAI. 8.2.2. Bacteria 8.2.2.1. Chlamydiaceae Chlamydophila psittaci causes ornithosis (chlamydiosis, also known as psittacosis) in gulls, pigeons, passerines and other birds, especially young ones. Adult birds are more resistant to the disease, but they can carry and intermittently shed the infectious agent for months (Roberts & Grimes, 1978). Clinical symptoms in birds are extremely variable, ranging from infection without symptoms to death caused by septicaemia. Some avian species may remain serologically negative despite active chlamydiosis. The importance of chlamydiosis to the population dynamics of wild birds is probably underrated. Epizootic episodes of disease – that is, the rapid spread among animals – with high mortality have been described; such episodes have occurred in gulls in North America (Brand, 1989). Also, C. psittaci was isolated from synanthropic species such as mallards, herring gulls (Larus argentatus), black-headed gulls, feral pigeons, wood pigeons (Columba palumbus), collared doves, common starlings and house sparrows (Strauss, Bednáˇr & ˇSer´y, 1957; ˇSer´y & Strauss, 1960; Illner, 1961; Terskikh, 1964; Davis et al., 1971; Wobeser, 1997; Odermatt et al., 1998; Gautsch et al., 2000; Dovc et al., 2004; Haag-Wackernagel & Moch, 2004; Tanaka et al., 2005). Synanthropic doves, grackles and starlings may transmit C. psittaci to domestic birds (Grimes, Owens & Singer, 1979), and wild ducks, gulls and grackles may disperse the infectious agent (Page, 1976; Lvov & Ilyichev, 1979). The mean worldwide prevalence of C. psittaci in feral pigeons is 13% by isolation and 30% by serology (Davis et al., 1971), but as many as 38% and 56% of pigeons were found to be seropositive, for instance, in Slovakia and Switzerland, respectively (ˇReháˇcek & Brezina, 1976; Haag-Wackernagel & Moch, 2004). The feral pigeon plays a major role in the epidemiology of human ornithosis (Meyer, 1959; Terskikh, 1964; Sixl & Sixl, 1971; Sixl, 1975). At least 500 cases have been reported as acquired by people from feral pigeons or other synanthropic avian species in many parts of the world, often in urban conditions (Meyer, 1959; Henry & Crossley, 1986; Pospíˇsil et al., 1988; Wobeser & Brand, 1982; HaagWackernagel & Moch, 2004). 8.2.2.2. Coxiellaceae Coxiella burnetii, the causative agent of Q fever (also known as coxiellosis), was isolated from more than 40 species of wild birds, including synanthropic barn swallows (Hirundo rustica) and white wagtails (Motacilla alba) in the Czech Republic (Raˇska & Syr˚uˇcek, 1956), feral pigeons in Italy (Babudieri & Moscovici, 1952), house sparrows in central Asia and crows in India (Lvov & Ilyichev, 1979; ˇReháˇcek & Tarasevich, 1988). Pigeons and house sparrows are susceptible to experimental infection: they excrete C. burnetii in faeces, and the infectious agent is recoverable from the lungs, spleen and kidneys for 48–58 days post inoculation, while the birds do not develop any symptoms of the infection and are seronegative (Babudieri & Moscovici, 1952; Schmatz et al., 1977). Five members of a family living in southern France became ill with acute Q fever in May 1996, and an epidemiological investigation suggested that this outbreak resulted from exposure to contaminated pigeon faeces and their argasid ticks (Stein & Raoult, 1999). Also, the collared dove, a synanthropic species of dove with an expanding breeding range, has been suggested to be responsible for the introduction of the Q fever to Ireland (ˇReháˇcek & Tarasevich, 1988). 8.2.2.3. Anaplasmataceae Anaplasma phagocytophilum, the causative agent of human granulocytic anaplasmosis (previously known as human granulocytic ehrlichiosis), can be carried in immature deer ticks (Ixodes scapularis) and castor-bean ticks attached to such synanthropic birds as some turdids, as it was detected in North America (Daniels et al., 2002), European parts of the Russian Federation (Alekseev et al., 2001) and Sweden (Bjoersdorf et al., 2001). However, no Anaplasma infections of people have been reported as attributable to, or directly associated with, urban birds. 8.2.2.4. Spirochaetaceae Borrelia burgdorferi s.l., the causative agent of Lyme borreliosis, was repeatedly detected in preimaginal deer and castor-bean vector ticks collected from birds, including synanthropic species of the American robin (Turdus migratorius), the common blackbird, and the song thrush in North America and Europe (Anderson et al., 1986; Magnarelli, Stafford & Bladen, 1992; Humair et al., 1993; Hubálek, Juˇricová & Halouzka, 1995; Hubálek et al., 1996; Hanincová et al., 2003, Stern et al., 2006). Tick larvae and nymphs have parasitized some species of birds as frequently as they have parasitized the whitefooted mouse (Peromyscus leucopus), the principal reservoir host of B. burgdorferi s.s. in North America. Bird-feeding larval and nymphal deer ticks were removed from their hosts, left to molt, and shown to transmit B. burgdorferi transstadially (that is, from one stage of the life-cycle to the next) into the adult stage (Anderson, Magnarelli & Stafford, 1990). In Switzerland, 16% of larval and 22% of nymphal castor-bean ticks collected from passerine birds were infected with borreliae; the highest infection rate was observed in ticks removed from thrushes (Turdidae) (Humair et al., 1993). In the Czech Republic, borreliae were detected in 7% of larval and 12% of nymphal castor-bean ticks collected from wild birds; positive ticks were collected from synanthropic species: the common blackbird, the European robin (Erithacus rubecula) and the great tit. Three massively infected ticks with hundreds of borreliae were collected from robins and blackbirds, and Borrelia garinii was isolated from a nymphal tick, collected from a young blackbird (Hubálek et al., 1996). A high rate of infection with borreliae (mainly B. garinii and Borrelia valaisiana) was also found in preimaginal ticks, collected from Turdidae in Slovakia (Hanincová et al., 2003). Moreover, some synanthropic bird species are competent amplifying hosts for B. burgdorferi s.l. – for instance, the common blackbird (Humair et al., 1998) and the American robin (Richter et al., 2000; Ginsberg et al., 2005). However, no B. burgdorferi s.l. infections of people have been reported as attributable to, or directly associated with, urban birds. 8.2.2.5. Campylobacteraceae Campylobacter jejuni is the most frequently isolated Campylobacter spp. from a wide variety of aquatic and terrestrial wild birds (including synanthropic anatids, gulls, pigeons, corvids, starlings and sparrows), followed by Campylobacter coli and C. laridis (Rosef, 1981; Kapperud & Rosef, 1983; Kinjo et al., 1983; Kaneuchi et al., 1987; Mégraud, 1987; Whelan et al., 1988; Glünder & Petermann, 1989; Maruyama et al., 1990; Glünder et al., 1991; Quessy & Messier, 1992; Sixl et al., 1997; Odermatt et al., 1998; Gautsch et al., 2000; Haag-Wackernagel & Moch, 2004). Campylobacter spp. cause either asymptomatic carriership in adult birds or signs of anorexia, diarrhoea and (occasionally) mortality in fledglings. Among birds found in the city of Oslo, very high isolation rates of Campylobacter spp. were detected (Kapperud & Rosef, 1983) in omnivorous and scavenging species: carrion crows (90%), herring gulls (50%) and black-headed gulls (43%). C. jejuni was also recovered from 3% and 14% of feral pigeons in Norway and Croatia, respectively (Lillehaug et al., 2005; Vlahoviˇc et al., 2004). As many as 46% of Japanese crow (also known as jungle crow, Corvus levaillantii) and carrion crow dropping samples contained C. jejuni, mostly biovar I serogroup 2, reflecting a close epidemiological association between the crow and human isolates (Maruyama et al., 1990). Campylobacter spp. are transmissible to other birds through droppings and aerosols. The carrier state of young black-headed gulls for C. jejuni has been shown to last for about 3–4 weeks (Glünder, Neumann & Braune, 1992). Campylobacter jejuni and C. coli cause human campylobacterosis (food-borne enterocolitis) worldwide, but some avian biotypes are distinct from human isolates. In C. jejuni isolated from 53% of pigeon faecal samples in the Bordeaux region of France; the main biotype was I – that is, the most common biotype in human disease (Mégraud, 1987). Seagulls and common grackles (Quiscalus quiscula) were implicated in the indirect spread of Campylobacter spp. to domestic animals and people, via feedstuffs and water, respectively (Sacks et al. 1986). Jackdaws (Corvus monedula) and European magpies (Pica pica) caused a milk-borne Campylobacter epidemic (with 59 human cases) by pecking milk bottles in England (Hudson et al., 1991). 8.2.2.6. Enterobacteriaceae 8.2.2.6.1. Escherichia Escherichia coli enteropathogenic strains, such as serotype O157:H7 (which produces verotoxin or Shiga-like toxin), have quite often been isolated from healthy and ill wild synanthropic birds, such as the feral pigeon (Haag-Wackernagel & Moch, 2004; Grossmann et al., 2005), the wood pigeon (McDiarmid, 1969), the Canada goose (Branta canadensis) (Hussong et al., 1979), the common starling (Nielsen et al., 2004) and seagulls (Makino et al. 2000) and from nestlings, dead embryos and eggs of Passer spp. (Pinowski, Kavanagh & Górski, 1991). In addition, wild urban birds may become the carriers of E. coli strains resistant to antibiotics and may be responsible for the spread of R plasmids (the extrachromosomal self-replicating structures sometimes found in bacterial cells that carry the genetic information for antibiotic resistance) in a wide area (Kanai, Hashimoto & Mitsuhashi, 1981). However, no enteropathogenic E. coli infections of people have been reported as attributable to, or directly associated with, urban birds. 8.2.2.6.2. Salmonella Numerous Salmonella enterica serovars, particularly Typhimurium and Enteritidis were isolated from many species of synanthropic birds, such as gulls, pigeons, sparrows, starlings and corvids, and some may present a potential threat to the health of domestic animals and the health of people (Keymer, 1958; Nielsen, 1960; Snoeyenbos, Morin & Wetherbee, 1967;Wilson & Macdonald, 1967; Pohl & Thomas, 1968; Cornelius, 1969; McDiarmid, 1969; Tizard, Fish & Harmerson, 1979; Niida et al., 1983; Simitzis-le Flohic et al., 1983; Odermatt et al., 1998; Toro et al., 1999; Gautsch et al., 2000; Dovc et al., 2004; Haag-Wackernagel & Moch, 2004). Many authors reported the isolation of Typhimurium, Enteritidis and other Salmonella serovars from synanthropic gulls – such as black-headed gulls, herring gulls/Caspian gulls (Larus cachinnans) and California and ring-billed gulls (Larus californicus and Larus delawarensis, respectively) – in Europe or North America (Strauss, Bednáˇr & ˇSer´y, 1957; ˇSer´y & Strauss, 1960; Nielsen, 1960; Petzelt & Steiniger, 1961; Snoeyenbos, Morin & Wetherbee, 1967; Müller, 1970; Berg & Anderson, 1972; Pannwitz & Pulst, 1972; Wuthe, 1972, 1973; Fennel, James & Morris, 1974; Macdonald & Brown, 1974; Pagon, Sonnabend & Krech, 1974; Williams, Richards & Lewis, 1976; Hall et al., 1977; Plant, 1978; Fenlon, 1981, 1983; Benton et al., 1983; Butterfield et al., 1983; Kapperud & Rosef ,1983; Fricker, 1984; Girdwood et al., 1985; Literák & Kraml, 1985; Monaghan et al., 1985; Glünder, Siegmann & Köhler, 1991; Glünder et al., 1991; Selbitz et al., 1991; Literák et al., 1992; Quessy & Messier, 1992; Lévesque et al., 1993; Hubálek, Juˇricová & Halouzka, 1995). Gulls could thus play a significant role in dispersing pathogenic salmonellae, even in urban areas. Salmonellae (Typhimurium, Enteritidis, Paratyphi B serovars) have been recovered repeatedly from feral pigeons or synanthropic sparrows (Petzelt & Steiniger, 1961; Dózsa, 1964; Wobeser & Finlayson, 1969; Tizard, Fish & Harmerson, 1979; Tanaka et al., 2005). In pigeons, the serovar Typhimurium var. copenhagen is especially common, and its cells are usually firmly attached to the duodenal epithelium of the birds, causing long-term or persistent infection (Grund & Stolpe, 1992). A number of house sparrows from 36 sites in Poland were examined: the prevalence of salmonellae (serovars Typhimurium, Dublin and Paratyphi B) varied from 0% to 40% (Pinowska, Chylinski & Gondek, 1976). Certain Salmonella serovars can cause lethal enteritis and hepatitis of nestlings, especially gulls and other colonial water birds; the serovars Gallinarum and Typhimurium were encountered among the causes of death in British sparrows (Keymer, 1958; Baker, 1977). Experimental infection of the fledgling house sparrow with the serovar Typhimurium resulted in a rather severe disease, while some birds remained relatively asymptomatic, but excreted the salmonellae (Stepanyan et al., 1964). Epizootic episodes of salmonellosis with high mortality caused by the serovar Typhimurium have repeatedly been described among sparrows, greenfinches and other urban passerines at bird feeders in Europe and North America, particularly during the winter and spring (Englert et al., 1967; Wilson & Macdonald, 1967; Bouvier, 1969; Cornelius, 1969; Schneider & Bulling, 1969; Greuel & Arnold, 1971; Locke, Shillinger & Jareed, 1973; Nesbitt & White, 1974; Macdonald, 1977; Brittingham & Temple, 1986; Bowes, 1990; Tizard, 2004). Garden bird feeders can become heavily contaminated with salmonellae (serovar Typhimurium), and the infected birds may transmit the infection to people (directly or via cats feeding on them: Tizard, 2004). Also, an epornitic of salmonellosis occurred in common starlings overwintering in Israel (Reitler, 1955). Osteomyelitic and arthritic salmonellosis was described in carrion crows (Daoust, 1978) and pigeons, and cutaneous salmonellosis was described in house sparrows (Macdonald, 1977). Human cases of salmonellosis were reported after the handling of injured gulls (Macdonald & Brown, 1974) or drinking water contaminated by gulls (Benton et al., 1983), even in urban areas. 8.2.2.6.3. Yersinia Yersinia enterocolitica infects wild anatids, gulls, pigeons, and some passerines (Mair, 1973; Hacking & Sileo, 1974; Kapperud & Olsvik, 1982; Simitzis-le Flohic et al., 1983; Shayegani et al., 1986; Kaneuchi et al., 1989; Odermatt et al., 1998; Gautsch et al., 2000). In the United States, 3% of wild avian faecal samples were positive for Y. enterocolitica, but no serogroup O:8 or O:3 human pathogenic isolates were recovered (Shayegani et al., 1986). The isolation rate in Japan for Y. enterocolitica was higher, at 7% (Kato et al. 1985). The avian hosts are usually asymptomatic, but sometimes the clinical signs include anorexia, diarrhoea and weight loss. Unlike Yersinia pseudotuberculosis, Y. enterocolitica is less frequent in birds than in humans, and there is no evidence that birds are significant reservoirs for it. No Y. enterocolitica infections of people have been reported as attributable to, or directly associated with, urban birds. Yersinia pseudotuberculosis can cause mortality in wild birds, including such synanthropic species as the wood pigeon, Passer spp., the barn swallow, the common starling, the common grackle, the common blackbird, the jackdaw, the rook and the American crow (Jennings, 1955–1957; Keymer, 1958; Jennings, 1959, 1961; Clark & Locke, 1962; McDiarmid, 1969; Lipaev et al., 1970; Davis et al., 1971; Mair, 1973; Hacking & Sileo, 1974). Avian pseudotuberculosis sometimes occurs in epizootic episodes (especially during severe winter conditions), and its manifestations are varied: ruffled feathers, anorexia, diarrhoea, lack of coordination and sudden death. Some wild avian species, however, are known to be refractory to natural infection. Isolations of Y. pseudotuberculosis were reported from healthy synanthropic birds: common starlings in France and Switzerland (Simitzis-le Flohic et al., 1983; Odermatt et al., 1998; Gautsch et al., 2000), and pied wagtails in Japan (Fukushima & Gomyoda, 1991). Gulls were also found to be infected in the Far East (Lvov & Ilyichev, 1979; Kaneuchi et al., 1989). For people, free-living birds that carry and shed the causative agent via faeces may represent a source of infection. In Japan, Y. pseudotuberculosis isolates from wild ducks were of serotypes 1b and 4b, which represent the most frequent serovars in local human strains, and they contained the same plasmid types (3 and 1, respectively) as human isolates (Hamasaki et al., 1989; Fukushima & Gomyoda, 1991). 8.2.2.7. Gram-positive cocci 8.2.2.7.1. Staphylococcus Staphylococcus aureus (Micrococcaceae) was isolated from the faeces of gulls (Cragg & Clayton, 1971), corvids (Golebiowski, 1975; Hájek & Balusek, 1988) and other synanthropic birds (Keymer, 1958). Staphylococcosis associated with trauma caused the death of a house sparrow (Keymer, 1958), and a mixed fungal cutaneous infection with S. aureus was described in the same species (Hubálek, 1994). Staphylococcal arthritis in gulls and necrotic arthritic lesions on the feet of European robins were observed in England (Macdonald, 1965; Blackmore & Keymer, 1969). Staphylococcus aureus was also isolated from 14% of dead wild birds (such as asserines) in England (Harry, 1967), dead embryos and eggs of sparrows in Poland (Pinowski, Kavanagh & Górski, 1991: together with S. epidermidis). Staphylococcal foot dermatitis (an inflammation of the ball of the foot of fowls, called bumblefoot) has been reproduced experimentally in common starlings infected with S. aureus (Cooper & Needham, 1981), and from that species the causative agent was also isolated (Odermatt et al., 1998; Gautsch et al., 2000). A disseminated S. aureus infection caused the death of four mallards overwintering in Saskatchewan (Wobeser & Kost, 1992). Also, a number of coagulase-positive staphylococcal strains from synanthropic birds (such as pigeons, rooks, gulls and ducks) have been shown to represent Staphylococcus intermedius (Hájek & Balusek, 1988; Hájek et al., 1991). However, no infections of people with Staphylococcus spp. have been reported as attributable to, or directly associated with, urban birds. 8.2.2.7.2. Streptococcus Streptococcus bovis has been described as an important cause of septicaemia in pigeons of all ages (Devriese et al., 1990). In Belgium, the causative agent was frequently isolated from both healthy pigeons carriers) and those dead from septicaemia. Streptococcus bovis strains from pigeons were of biotypes similar to ovine and bovine strains, but differed from those isolated from human beings (De Herdt et al., 1995). Another streptococcus, of group C, was isolated from great tits and common starlings (Jennings, 1955–1957, 1959). However, no S. bovis infections of people have been reported as attributable to, or directly associated with, urban birds. 8.2.2.8. Regular nonsporing Gram-positive rods 8.2.2.8.1. Listeria Listeria monocytogenes, the etiological agent of listeriosis, can cause sporadic septic cases of the disease even in wild birds, such as common starlings and European robins (Macdonald, 1968; McDiarmid, 1969). Faecal samples from synanthropic gulls that fed at Scottish sewage works had a higher rate of carriage of the infectious agent (15%) than those species that fed elsewhere (4%); the infection rate of rooks was generally lower (6%) (Fenlon, 1985). Also, gulls may play a significant role in contaminating silage with members of the genus Listeria. Listeria monocytogenes was isolated from healthy synanthropic collared doves and house sparrows in the Czech Republic (Treml et al., 1993) and from roosting starlings in Switzerland (Odermatt et al., 1998; Gautsch et al., 2000). However, no infections of people have been reported as attributable to, or directly associated with, urban birds. 8.2.2.8.2. Erysipelothrix Erysipelothrix rhusiopathiae, the etiological agent of erysipeloid in man, which is a localized, self-limited cutaneous lesion, can cause epornitics and even mass mortality in waterbirds. Other cases have included gulls in Denmark, pigeons, wild ducks and thrushes in Germany, and starlings in the United States (Faddoul, Fellows & Baird, 1968; Macdonald, 1968; McDiarmid, 1969). However, no E. rhusiopathiae infections of people have been reported as attributable to, or directly associated with, urban birds. 8.2.2.9. Mycobacteriaceae Mycobacterium avium causes tuberculosis (mycobacteriosis) in many wild avian species, including synanthropic columbiforms, sparrows, corvids, gulls and anatids (Plum, 1942; Mitchell & Duthie, 1950; Jennings, 1955–1957, 1959; Keymer, 1958; Jennings, 1961; Brickford, Ellis & Moses, 1966; ˇSvrˇcek et al., 1966; Blackmore & Keymer, 1969; McDiarmid, 1969; Davis, et al., 1971; Schaefer et al., 1973; Baker, 1977; Wobeser, 1997; Smit et al., 1987; Hejlíˇcek & Treml, 1993a–c). It is one of the most widespread wild avian infections, often resulting in a marked weight loss, severe muscle atrophy and death. Some synanthropic birds (such as wood pigeons in England, house sparrows and rooks elsewhere) could be carriers of M. avium and could play a role in the spread of avian tuberculosis to poultry and domestic animals (Kubín & Matˇejka, 1967). Plum (1942) examined 1000 house and tree sparrows from 40 farms in Denmark and found M. avium in 9% of them; tuberculous lesions were present in 2% of the birds. Several strains of M. avium were isolated from Passer spp. in the Czech Republic; the birds were considered a possible source of tuberculosis infection in cattle (Matˇejka & Kubín, 1967; Rossi & Dokoupil, 1967; Hejlíˇcek & Treml, 1993a, c). In the Czech Republic, infected chickens are the main source of mycobacteria for house sparrows (Hejlíˇcek & Treml, 1993a, c). Mycobacterium avium was also isolated from a collared dove (Volner, 1978); in experiments, this dove species was found to be much less susceptible than the chickens, but could be a potential carrier of the infectious agent (Rossi, 1969; Hejlíˇcek & Treml, 1993b). Mycobacteria, including M. avium-intracellulare complex, were detected in 19% of 153 faecal samples of feral pigeons collected in Japan (Tanaka et al., 2005). However, biological and molecular typing (sometimes even nucleotide sequencing) of M. avium strains from free-living birds seems to be necessary for a proper epidemiological evaluation of the birds as sources of human infections – that is, to compare the avian and clinical human isolates closely and to detect whether they are identical or not (Schaeffer et al., 1973; McFadden et al., 1992). Also, there are a few unconfirmed, anecdotal cases of M. avium clinical infections of people (ornithologists) who collected and examined urban owl and raptor pellets. Mycobacterium xenopi was occasionally found to cause human disease – for example, a nosocomial outbreak in Le Havre, France, where 558 cases were diagnosed for the period 1965–1967; free-living birds were the probable source of the outbreak, and the causative agent was isolated from droppings of local tree sparrows and common blackbirds (Joubert, Desbordes-Lize & Viallier, 1971). Other mycobacteria potentially pathogenic to people (M. avium-intracellulare, M. aquae, M. flavescens and M. fortuitum) were isolated from rooks (Kubín & Matˇejka, 1967), anatids (Schaefer et al., 1973), gulls and jackdaws with necrosis in the liver and spleen (Smit et al., 1987). 8.2.3. Fungi 8.2.3.1. Yeasts and yeast-like fungi 8.2.3.1.1. Candida Candidosis (also called candidiasis and moniliasis) is, after aspergillosis, the second most significant mycosis of domestic and captive birds. In wild birds, however, the disease is virtually unknown, although C. albicans has often been isolated from the gastrointestinal tract and excretions of gulls (Kawakita & van Uden, 1965; Cragg & Clayton, 1971; Buck, 1983, 1990), pigeons and other wild birds (Littman & Schneierson, 1959; Frágner, 1962; Partridge & Winner, 1965; Brandsberg et al., 1969; Schönborn, Schütze & Pöhler, 1969; Kocan & Hasenclever, 1974; Hasenclever & Kocan, 1975; Gugnani, Sandhu & Shome, 1976; Refai et al., 1983; Pinowski, Kavanagh & Górski, 1991; Hubálek, 1994; HaagWackernagel & Moch, 2004), as well as from pellets of synanthropic rooks, nests of collared doves and feathers of house sparrows (Hubálek, 1994). Candida albicans seems to be especially frequent in fresh droppings of gulls: it was recovered from about half of the samples tested along the eastern coastline of the United States (Buck, 1983, 1990). Experimental observations of a gull fed fish containing C. albicans demonstrated a heavy shedding of the yeast via faeces for the next 13 days, and even 40 days post-feeding the gull excreted the yeast sporadically, even though it was treated with ketoconazole (Buck, 1986). The gulls may thus serve as carriers of C. albicans or as a reservoir for it. However, no C. albicans infections of people have been reported as attributable to, or directly associated with, urban birds. Other Candida spp. pathogenic to people have been isolated from a number of synanthropic wild avian samples (from excretions, the intestinal tract and other organs): Candida guilliermondii, Candida krusei, Candida tropicalis, Candida pseudotropicalis and Candida parapsilosis (Frágner, 1962; Kawakita & van Uden, 1965; Schönborn, Schütze & Pöhler, 1969; Cragg & Clayton, 1971; Kocan & Hasenclever, 1972; Monga, 1972; Gugnani, Sandhu & Shome, 1976; Guiguen, Boisseau-Lebreuill & Couprie, 1986; Pinowski, Kavanagh & Górski, 1991; Hubálek, 1994; Haag-Wackernagel & Moch, 2004). An outbreak of peritonitis due to C. parapsilosis in 12 patients undergoing peritoneal dialysis was attributed to contaminated pigeon excreta on window sills (Greaves et al., 1992). 8.2.3.1.2. Crypotococcus Avian (especially feral pigeon) excretions represent a significant natural source of cryptococcosis in people. The first isolation of C. neoformans (its teleomorph stage is Filobasidiella neoformans, a basidomycetous yeast) from the nests and droppings of feral pigeons (Emmons, 1955, 1960) was followed by a number of similar reports worldwide (Yamamoto, Ishida & Sato, 1957; Littman & Schneierson, 1959; Frágner, 1962; Tsubura, 1962; Bergman, 1963; Muchmore et al., 1963; Silva & Paula, 1963; Frey & Durie, 1964; Partridge & Winner, 1965; Procknow et al., 1965; Randhawa, Clayton & Riddell, 1965; Taylor & Duangmani, 1968; Hubálek, 1975; Gugnani, Sandhu & Shome, 1976; Refai et al., 1983; Ruiz, Vélez & Fromtling, 1989; Yildiran et al., 1998; Haag-Wackernagel & Moch, 2004; Chee & Lee, 2005). The association between C. neoformans var. grubii (formerly C. neoformans serotype A) and the feral pigeon is remarkable (Denton & Di Salvo, 1968), whereas the occurrence of the fungus in faeces of other wild bird species is surprisingly scarce. As many as a hundred thousand to a million viable C. neoformans cells have been detected per gram of pigeon excreta in different parts of the world (Emmons, 1960; Hubálek, 1975; Ruiz, Fromtling & Bulmer, 1981; Ruiz, Neilson & Bulmer, 1982; Ruiz, Vélez & Fromtling, 1989). This association was shown to be conditioned nutritionally, due to the ability of the yeastlike organism to utilize all basic low-molecular-weight nitrogenous substances from avian urine – that is, uric acid, creatinine, xanthine, guanine and urea – and due to the tenacity of the causative agent, C. neoformans (Staib, 1962, 1963; Walter & Yee, 1968; Hubálek, 1975; Ruiz, Neilson & Bulmer, 1982). The birds (pigeons) serve therefore largely as a lessor (Hubálek, Juˇricová & Halouzka, 1995) for the fungus. However, carriage of the fungus has also been proved by isolating it from the feet and bills of feral pigeons (Littman & Borok, 1968) or from their lower and upper digestive tracts (Sethi & Randhawa, 1968; Swinne-Desgain, 1976; Khan et al., 1978; Guiguen, Boisseau-Lebreuill & Couprie, 1986; Rosario et al., 2005). In an experiment, pigeons with C. neoformans administered into the crop excreted the fungus sporadically in faeces up to 22 days, but harboured it for at least 86 days in the crop (Swinne-Desgain, 1976); this study demonstrated that pigeons could carry the fungus in their upper digestive tract. Spontaneous (natural) cryptococcosis has only rarely been observed in feral columbiforms (Hermoso de Mendoza et al., 1984). The course of experimental avian infections is usually abortive; only intracerebral inoculation was sufficient to cause death in some pigeons; the agent persisted in the brain for up to 11 weeks (Littman, Borok & Dalton, 1965; Böhm et al., 1974). The low susceptibility of birds to cryptococcosis may be due to the poor or nil growth of the fungus at 41°C – that is, at the avian body temperature. There are several reports on human cryptococcal meningitis or pneumonia acquired by contact with pigeon habitats contaminated with the infectious agent (Muchmore et al., 1963, Procknow et al., 1965). Cryptococcus neoformans has been repeatedly isolated – even from the air – in feral pigeons’ breeding sites (Staib & Bethäuser, 1968; Powell et al., 1972; Ruiz & Bulmer, 1981; Ruiz, Neilson & Bulmer, 1982), and the cell size of airborne yeastlike particles (0.6–3.5µm) is compatible with alveolar deposition after inhalation. Some studies have found that antibodies to C. neoformans are more frequent in people who have been in contact with pigeons than in people of the control group (Walter & Atchison, 1966; Newberry et al., 1967). Nearly all isolates from pigeon excreta are of serotype A (C. neoformans var. grubii), the same as most strains isolated from human cases of cryptococcosis (Walter & Coffee, 1968). The incidence of human cryptococcosis is 5–30% in patients with AIDS (or in people who are HIV-positive); a study from Burundi indicated that many of these cases could have acquired the mycosis by contact with contaminated pigeon habitats (Swinne et al., 1991). In Australia, a man died from cryptococcal meningitis four months after removing a Welcome swallow (Hirundo neoxena) nest heavily contaminated with C. neoformans serotype A from the roof (Glasziou & McAleer, 1984). A human case of osteomyelitis caused by C. neoformans var. grubii was described in Sweden; the patient became infected by cleaning a wooden box that had been used for several consecutive years for breeding by starlings and that contained the infectious agent (Kumlin et al., 1998). 8.2.3.2. Ascomycetes 8.2.3.2.1. Histoplasma Histoplasma capsulatum (teleomorph Ajellomyces capsulatus) has occasionally been isolated from pigeon excreta and feathers (Suthill & Campbell, 1965). However, the most important source of human histoplasmosis in urban ecosystems of North America are roosting sites for common starlings and blackbirds (mostly the red-winged blackbird (Agelaius phoeniceus) and common grackle), which are often occupied by tens of thousands of these birds. In such sites, the ground under the trees is covered with a thick layer of droppings, becoming a habitat of H. capsulatum for years, and the soil is a source of human infection (Furcolow et al., 1961; Murdock et al., 1962; Ajello, 1964; Dodge, Ajello & Engelke, 1965; Tosh et al., 1966, 1970; Younglove et al., 1968; Brandsberg et al., 1969; Storch et al., 1980). Like C. neoformans, H. capsulatum can grow in bird droppings, by utilizing uric acid (the main and specific constituent of avian urine) (Vanbreuseghem & Eugene, 1958; Smith, 1964, 1971; Lockwood & Garrison, 1968), and also on feathers (Suthill & Campbell, 1965). However, unlike C. neoformans, there is no reliable information that birds can carry H. capsulatum, and spontaneous histoplasmosis has not been confirmed in birds. Also, experimental inoculation of birds, even intraocular, did not cause disease (Schwarz et al., 1957; Sethi & Schwarz, 1966). Contaminated areas could pose a human health hazard for a prolonged period of time (Latham et al., 1980). For example, the endemic reactivity of children from a school in the United States to the skin-test antigen histoplasmin was ascribed to the presence of a nearby roosting site of blackbirds, the soil of which was the source of H. capsulatum (Dodge, Ajello & Engelke, 1965). Major outbreaks of histoplasmosis (300 human cases) occurred in Mason City, Iowa, following two repeated clearings (in 1962 and 1964) of a park area where large numbers of starlings had been roosting for years (D’Alessio et al., 1965; Tosh et al., 1966). A total of 355 students showed symptoms of histoplasmosis after the soil was rototilled in an Indiana school courtyard known as a blackbird–starling roosting site; H. capsulatum was then also isolated from filters in the school air-conditioning system (Chamany et al., 2004). In another case, children were infected through contact with a nesting place of common grackles, contaminated with the fungus. Also, a great number of people working on a ring-billed gull (Larus delawarensis) nesting colony site in winter developed acute pulmonary histoplasmosis, and H. capsulatum was isolated from the nesting site (Waldman et al., 1983). 8.2.4. Protozoa 8.2.4.1. Microsporidia (Note: Microsporidia have been newly classified as organisms closer to fungi than to protozoa) DNA from three microsporidian species – Enterocytozoon bieneusi, Encephalitozoon hellem and Encephalitozoon intestinalis – was recently detected in excreta of urban feral pigeons in Spanish parks (Haro et al., 2005). Children and the elderly are among the main visitors to these parks and, at the same time, they are the population groups at risk for microsporidiosis. However, no microsporidial infections of people have yet been reported as attributable to, or directly associated with, urban birds. 8.2.4.2. Babesiidae It is probable that the protozoan parasite Babesia microti, one of several infectious agents of human babesiosis, may occur on, and be dispersed by, some synanthropic birds via attached infected preimaginal deer and castor-bean vector ticks. However, no Babesia infections of people have yet been reported as attributable to, or directly associated with, urban birds. 8.2.4.3. Eimeriidae The protozoan parasite Toxoplasma gondii has been recorded relatively often in such wild birds as corvids (Finlay & Manwell, 1956; Lvov & Ilyichev, 1979; Literák et al., 1992), ducks, gulls (Lvov & Ilyichev, 1979; Literák et al., 1992) and columbids, including feral pigeons (Jacobs, Melton & Jones, 1952; Berger, 1966; Orlandella & Coppola, 1969; Lvov & Ilyichev, 1979; Literák et al., 1992; Haag-Wackernagel & Moch, 2004); it has been recorded less frequently in sparrows (Pak, 1976; Lvov & Ilyichev, 1979; Hejlíˇcek, Proˇsek & Treml, 1981; Literák et al., 1992), starlings (Pak, 1976; Haslett & Schneider, 1978; Lvov & Ilyichev, 1979; Peach, Fowler & Hay, 1989) and several other passerines (Pak, 1976; Hejlíˇcek, Proˇsek & Treml, 1981; Literák et al., 1992). On a communal roost in Leicester, England, 8% of starlings examined were infected; starlings could thus play an important role in the maintenance of toxoplasmosis in urban environments (Peach, Fowler & Hay, 1989). Infected starlings, sparrows and other small passerines can be the source of T. gondii infection for domestic cats. Many synanthropic avian species have shown to be susceptible to T. gondii when infected with it experimentally. For instance, pigeons inoculated with T. gondii have shown distinct clinical abnormalities (Biancifiori et al., 1986). Infected birds, such as pigeons, are less mobile and more susceptible to predation by cats which, as a definite host, could transmit the disease to other mammals, including human beings. On several occasions, pigeons were found to be the source of human toxoplasmosis (Orlandella & Coppola, 1969; Neto & Levi, 1970). 8.2.4.4. Cryptosporidiidae Cryptosporidium is an enteric intracellular coccidian parasite that causes gastrointestinal and respiratory tract disorders in birds, or (more often) subclinical and asymptomatic infections. Cryptosporidium oocysts were found in faeces and cloacal specimens of gulls (herring gulls and black-headed gulls) in Scotland (Smith et al., 1993), and Cryptosporidium baileyi has been detected very frequently in black-headed gulls (28–100% chicks positive) in the Czech Republic; respiratory cryptosporidiosis was also diagnosed in several young gulls (Pavlásek, 1993). However, no cryptosporidial infections of people have been reported as attributable to, or directly associated with, urban birds. 8.3. Zoonoses and sapronoses of wild birds in the urban ecosystem Although zoonoses of avian origin remain relatively infrequent (Cooper, 1990), many of the agents considered here (see Table 8.1) have been found to cause sporadic human cases or epidemics of corresponding zoonoses and sapronoses in urban areas, while others, though already established as associated with urban birds, have not yet been reported to cause infections in people attributable to, or directly caused by, urban birds. Nonetheless, vigilance is necessary, as the incidence of disease might be significantly underreported, and there might be a number of undiagnosed cases. Pathogens significantly associated with wild and feral birds in urban areas are, for example:
The ability of some fungi (less so of certain bacteria) to grow in avian excreta and nests is remarkable. These pathogens assimilate uric acid and other low-molecular-weight nitrogenous compounds contained in bird droppings, and the birds thus serve not as hosts for these microorganisms, but as lessors for them. This could pose a public health hazard in the case of mass communal roosts or large nesting colonies of birds at urban or suburban sites inhabited, exploited or attended by people. In these cases, airborne inhalation is the main means of infection in people, and it usually occurs during rebuilding or related work in contaminated areas. In general, the prevailing modes of transmission of pathogens from birds to people in urban areas are either via airborne or alimentary routes. An airborne, respiratory infection is the commonest mode in, for example, ornithosis, avian tuberculosis, cryptococcosis and histoplasmosis, while infection by ingestion might occur in, for example, salmonellosis, campylobacterosis, colibacillosis, listeriosis, toxoplasmosis and cryptosporidiosis, which are food-borne or water-borne diseases. Less frequently, some zoonotic infections in urban areas are transmitted by direct contact with birds, suffering from, for example, erysipeloid, streptococcosis, or pseudotuberculosis. Finally, arthropod-borne diseases (such as Eastern and Western equine encephalomyelitis, Sindbis fever, West Nile fever, TBE and Lyme borreliosis) are caused by haematophagous invertebrates (such as mosquitoes and ixodid ticks) that acquired the infectious agent previously, by feeding on viraemic or bacteraemic urban birds. A number of ecological factors might affect the risk of bird-borne illness in urban settings. For example, bird species that have higher population densities (such as feral pigeons); that nest in colonies (such as colonial waterbirds, gulls and rooks); that roost gregariously (such as starlings, grackles, corvids and gulls); and that congregate at water and food sources (such as terrestrial birds) or in other particular places in urban areas for mass moulting (such as waterfowl in summer), migration stops and overwintering (such as waterfowl and gulls) are more important epidemiologically (due to frequent interindividual contacts that enable effective horizontal transmission of disease agents) than species with low population densities that live solitarily or in small groups. Habitat preferences by birds also affect their epidemiological role. For example, aquatic birds, even in urban situations, attract higher numbers of haematophagous insects (such as mosquitoes) than do terrestrial birds, while woodland, ground-foraging birds are parasitized by ixodid ticks. Avian mobility and migratory habits are other crucial factors; they make the transport and spread of various agents by carrier birds more effective. In brief, the most important factors that increase the risk of bird-borne infections are:
8.4. Management implications 8.4.1. Benchmarks In general, the benchmarks for urban bird management should take into consideration the following (K. Sweeney, United States Environmental Protection Agency, personal communication, 2005):
This chapter has attempted to describe the recent state of knowledge of urban birds as a public health hazard. Some synanthropic avian species can obviously serve as hosts, reservoirs, transporters or lessors of a few human pathogens. However, the extent and significance of this epidemiological hazard might vary enormously, and it should be measured according to local conditions in particular urban areas. It is therefore very difficult to propose and apply a set of general benchmarks for urban birds as a public health threat. In general, the evidence and estimation of the level of threat must be based on data on the incidence of bird-borne illnesses in particular urban settings, using standard epidemiological surveillance methods. The straightforward way of determining the epidemiological hazard is to first establish whether a human bird-borne infection does or does not occur at a particular urban setting. If it does, the second step is to establish how often it occurs (incidence of the disease). The final step then involves a decision about the level (such as one human case or more cases) at which public funds should be spent on preventive and control programmes and measures. At least several cases of human disease directly associated with urban birds or their habitats have been reported for ornithosis, histoplasmosis, campylobacterosis, salmonellosis, mycobacteriosis, cryptococcosis, toxoplasmosis and Q fever (Table 8.1). However, compared with other communicable diseases, in general, their annual incidence is quite low, but underreporting should be taken into account. Also, although no cases acquired directly from birds have been described for a number of other infectious diseases (mostly arthropod-borne infections), certain wild urban birds can serve as amplifying hosts or carriers of infected preimaginal ixodid ticks, contributing thus to the circulation of disease agents in urban areas (Table 8.1). Moreover, allergic responses to ectoparasites of feral pigeons have not been included in Table 8.1 and are another consideration. 8.4.2. Monitoring and surveillance A prerequisite for managing urban birds and their potential public health hazard is the monitoring of avian populations and surveillance for associated zoonoses and sapronoses. The majority of the public health problems caused by wild birds are associated with feral pigeons, gulls, blackbirds, grackles, starlings, corvids and house sparrows. For instance, at least 800 reported transmissions of a pathogen (mostly C. psittaci) from feral pigeons to people have been found (Sixl, 1975; Pospíˇsil et al., 1988; Glünder, 1989; HaagWackernagel & Moch, 2004), this probably being only the so-called tip of the iceberg. Similarly, hundreds of cases of histoplasmosis in people have been acquired via the airborne route during, or after, work on communal roosts of birds in urban areas in North America (Furcolow et al., 1961; Murdock et al., 1962; Ajello, 1964; D’Alessio et al., 1965; Dodge, Ajello & Engelke, 1965; Tosh et al., 1966, 1970; Younglove et al., 1968; Latham et al., 1980; Storch et al., 1980; Waldman et al., 1983; Chamany et al., 2004). Public health surveillance should involve both a passive and active monitoring approach, the former based mainly on reports of disease, while the latter also includes serological surveys of urban birds and city dwellers, further microbiological examination of competent haematophagous invertebrate vectors and avian hosts (their infection rate), and investigations of habitats as sources of disease. Monitoring population density of the avian hosts and invertebrate vectors, and their spatial (mapping) and temporal (seasonal) distribution, is also necessary. Management priorities should then be established and objectives defined for prevention and control of bird-related infections. 8.4.3. Control of wild and feral birds in urban areas The control of wild bird populations (especially those of feral pigeons) in urban and suburban areas is difficult and sometimes ineffective. However, a few so-called publicfriendly methods are available to control potentially infected urban bird populations. To prevent risks that arise from the presence of infections in birds or infectious materials in their droppings, several tasks should be performed, as soon as microbiologists and epidemiologists have demonstrated an infection (zoonosis or sapronosis) (Lesaffre, 1997; Haag-Wackernagel, 1995, 2000; Rödl, 1999). These tasks include:
These activities should be carried out in an integrated approach to bird management, since individual steps alone do not produce success. Furthermore, inspection and control measures must be performed by, or under the supervision of, veterinary public health agencies – and only when they are substantiated and necessary. Ornithologists, wildlife managers and citizen representatives (such as consumers) should be involved in implementing the control measures. The integrated approach to bird management also needs a public education component (media) and a legal (regulatory) component – that is, political support – as necessary parts of the process. Finally, a risk–benefit analysis should also be performed. 8.4.4. Techniques for dispersing birds in cities Birds can be dispersed by various techniques (Frings & Jumber, 1954; Bickerton & Chapple, 1961; Schmitt, 1962; Brough, 1969; Gorenzel & Salmon, 1992, 1993). Briefly, they include the use of:
Birds, however, usually get accustomed to being disturbed by various acoustic or light signals. Some of the methods could be used only under certain circumstances and should be used respectfully in residential environments. 8.4.5. Economic impact of wild urban birds on human health and of controlling birds The financial costs of bird-borne diseases that affect people in urban areas are extremely difficult to estimate at present. Some reasons for this are as follows.
In any economic analysis on this issue, there will always be a very significant margin of error, in that there are no exact data available. So for now, even estimates by experts will be of limited value. Followed by acknowledgement and references; section "9. Human body lice" doesn't mention pigeons 10. Ticks Summary The most common vector-borne diseases in both Europe and North America are transmitted by ticks. Lyme borreliosis (LB), a tick-borne bacterial zoonosis, is the most highly prevalent. Other important tick-borne diseases include TBE (tick-borne encephalitis) and Crimean-Congo haemorrhagic fever in Europe, Rocky Mountain spotted fever (RMSF) in North America, and numerous less common tick-borne bacterial, viral, and protozoan diseases on both continents. The major etiological agent of LB is Borrelia burgdorferi in North America, while in Europe several related species of Borrelia can also cause human illness. These Borrelia genospecies differ in clinical manifestations, ecology (for example, some have primarily avian and others primarily mammalian reservoirs), and transmission cycles, so the epizootiology of LB is more complex in Europe than in North America. Ticks dwell predominantly in woodlands and meadows, and in association with animal hosts, with only limited colonization of human dwellings by a few species. Therefore, suburbanization has contributed substantially to the increase in tick-borne disease transmission in North America by fostering increased exposure of humans to tick habitat. The current trend toward suburbanization in Europe could potentially result in similar increases in transmission of tick-borne diseases. Incidence of tick-borne diseases can be lowered by active public education campaigns, targeted at the times and places of greatest potential for encounter between humans and infected ticks. Similarly, vaccines (e.g., against TBE) are most effective when made available to people at greatest risk, and for high-prevalence diseases such as LB. Consultation with vector-borne disease experts during the planning stages of new human developments can minimize the potential for residents to encounter infected ticks (e.g., by appropriate dwelling and landscape design). Furthermore, research on tick vectors, pathogens, transmission ecology, and on geographic distribution, spread, and management of tick-borne diseases can lead to innovative and improved methods to lower the incidence of these diseases. Surveillance programs to monitor the distribution and spread of ticks, associated pathogens, and their reservoirs, can allow better-targeted management efforts, and provide data to assess effectiveness and to improve management programs. 10.1. Introduction Ticks transmit more cases of human disease than any other arthropod vector in Europe and North America. They are also important worldwide as disease vectors to people and domestic animals, and they cause substantial economic losses, both by transmitting disease and by direct negative effects on cattle (Jongejan & Uilenberg, 2004). Lyme borreliosis (LB), in particular, is the most commonly reported vector-borne disease in both Europe and North America (Steere, Coburn & Glickstein, 2005). In Europe, Tick-Borne Encephalitis is also prevalent, especially in central and eastern Europe, while in North America, Rocky Mountain spotted fever (RMSF), caused by a rickettsial agent, is responsible for a few hundred to over a thousand cases a year. In addition to their importance as disease vectors, some hard tick species can directly cause adverse effects, such as tick paralysis, a toxicosis (systemic poisoning) due to toxic salivary proteins. Similarly, soft ticks can provoke severe allergenic bite reactions in people (IgE-mediated type-I allergy). The response to tick-borne diseases (TBDs) in the United States has been substantial, including federally sponsored research programmes, public health programmes within individual states (partly funded by the CDC [United States Centers for Disease Control and Prevention]) and several smaller programmes funded by states, localities and nonprofit-making organizations. States with a high incidence of disease have numerous public education programmes, and several novel methods of tick and disease management have been developed (Stafford & Kitron, 2002). However, coordination and evaluation of programmes is spotty, and the incidence of disease remains high in many locales and has increased nationwide (Piesman & Gern, 2004). Ecological differences in transmission dynamics from site to site mean that the approach to management needs to be tailored to conditions at each locale. Methods for developing effective IPM programmes and evaluations of efficacy remain high priorities (Ginsberg & Stafford, 2005). The situation in Europe is different in that national reporting strategies differ among countries (Table 10.1), and little has been done to routinely implement measures that protect individuals against tick bites or TBDs. Some notable exceptions are vaccination against TBE (Nuttall & Labuda, 2005) and the use of skin repellents in some areas. Fabrics impregnated with acaricides (agents that kill ticks and mites), such as permethrin, are widely unknown and difficult to procure, even for personnel occupationally exposed to tick-infested areas of endemic TBDs. So far, few research efforts have been initiated to reduce tick populations by ecological changes, biological control or IPM. 10.2. Ticks of Europe and North America Ticks are arachnids (the class Arachnida includes spiders, scorpions, ticks and mites) in the subclass Acari, which includes mites and ticks. There are three families of ticks (Barker & Murrell, 2004): the hard ticks, Ixodidae (713 species), which includes most ticks of medical importance to people; the soft ticks, Argasidae (185 species), which includes a few species that transmit diseases to humans; and Nuttalliellidae, which includes just one species from Africa with no known medical importance. Endemic tick species in Europe can be peridomestic or can be associated with pets and farm animals (Table 10.2). European ticks that can infest buildings in urban environments include: the ixodid brown dog tick, Rhipicephalus sanguineus, as far north as southern Germany; and the argasids: the European pigeon tick, Argas reflexus (associated with pigeons), and the fowl tick, Argas persicus (associated with poultry in south-eastern Europe). Long-term infestations with brown dog ticks can occur in human dwellings, if control efforts are neglected (Gothe, 1999). The only survey thus far for European pigeon ticks was performed in the city of Berlin, where more than 200 infested buildings were discovered between 1989 and 1998 (Dautel, Scheurer & Kahl, 1999). Most of the infestations were found in older buildings constructed before 1918. Control is difficult and requires professional expertise and time. Recent studies in Germany have shown increases in urban and periurban collections of castor-bean ticks, Ixodes ricinus (Mehnert, 2004). According to studies conducted in northeastern Germany, Lyme borreliosis (LB) is most often acquired in city parks and gardens near forests (Ammon, 2001; Anonymous, 2005a). Other ticks, such as the soft tick Ornithodoros erraticus, and the hard ticks Dermacentor spp., Hyalomma spp. and Haemaphysalis spp., are associated with pigs, sheep and cattle and are known vectors of both animal and human disease agents. They usually do not infest houses, but can be found in stables and in houses that incorporate stables. The most common hard ticks that regularly bite people in North America (Table 10.3) include: the black-legged or deer tick, Ixodes scapularis, in eastern and central North America; the western black-legged tick, Ixodes pacificus, in west coastal areas; the American dog tick, Dermacentor variabilis, in the east and Midwest; the Rocky Mountain wood tick, Dermacentor andersoni, in the Rocky Mountain region; the Pacific Coast tick, Dermacentor occidentalis, on the Pacific coast; and the lone star tick, Amblyomma americanum, in eastern and central North America. The brown dog tick attaches to dogs and can be found in the home, but rarely attaches to people. The primary soft ticks that affect people are Ornithodoros spp. in western areas. These ticks are found primarily in natural areas and are often encountered by recreational users of parks and woodlands (Ginsberg & Ewing, 1989). However, increasing suburbanization around major urban centres has resulted in substantial contact between people and ixodid ticks, and most disease transmission from ticks to people occurs in the peridomestic environment (Maupin et al., 1991). Some nidicolous species (including soft ticks, such as Ornithodoros spp.) are found in animal nests in rustic cabins and can transmit pathogens (such as relapsing fever borreliae) to recreational users of these dwellings (Barbour, 2005). 10.3. Tick-borne diseases The epidemiology and distribution of TBDs in Europe and North America are generally similar, but differ in some important details. In Europe, 31 viral, 14 bacterial, and 5 Babesia species are known endemic tick-borne pathogens of people (Table 10.4). Among European TBDs, only TBE is a widely notifiable disease (Table 10.1), with more than 10000 clinical cases annually. Detailed epidemiological information is not available on other TBDs, despite the fact that the most frequent TBD in Europe is LB (with possibly hundreds of thousands of clinical cases a year). Germany alone claims 20 000–60 000 cases a year (O’Connell et al., 1998; Wagner, 1999). Yearly rates of incidence in hyperendemic foci (sites where disease organisms exist in host populations at very high rates) can exceed 300 cases per 100 000 population, with average occupational seroprevalence rates of up to 48% in forest workers. Other TBDs occur, but their rates of incidence remain largely unknown. Several isolated regional studies in Europe show that tick abundance is increasing regionally while TBDs are simultaneously emerging and spreading geographically. The changing urban landscape in Germany, specifically in the federal state of Brandenburg, where LB has been a notifiable disease since 1996, shows a steady increase in exposure to castorbean ticks. Other studies have shown that urban parks in Berlin and Munich have growing tick populations and contribute to a growing number of cases of LB. In the Czech Republic, castor-bean tick populations spread an average of 161 meters into higher altitude sites (from about 780m to 960m above sea level) during the last 30 years. This resulted in exposure to ticks and TBDs in higher mountainous areas that were formerly not endemic for castor-bean ticks and diseases associated with them. Since the 1990s at least two TBDs, TBE and Mediterranean spotted fever (MSF), have been reported to be extending their geographical ranges. TBE is spreading geographically into the north-eastern parts of Germany. MSF, transmitted by the brown dog tick, is reportedly spreading northwards along the French Rhone Valley, as far north as Belgium, where the first autochthonous (locally acquired) human cases of MSF were recently reported. Data from the Baltic states show that landscape-level ecological changes (resulting from agricultural practices) have led to increases in ecotopes (the smallest ecologically distinct features in a landscape mapping and classification system) suitable for tick infestation. Finally, the reported increase in incidence of TBDs may in part result from increased awareness of TBDs, better diagnostic tools, and markedly higher leisure and sporting activities that result in increased exposure to endemic disease foci. The most common TBD in North America, as in Europe, is Lyme borreliosis (also called Lyme disease). Other important TBDs (Sonenshine, Lane & Nicholson, 2002) include RMSF, human monocytic ehrlichiosis (HME), human granulocytic anaplasmosis (HGA), Q fever, and tularaemia (Table 10.5). All of these diseases are notifiable in the United States (Groseclose et al., 2004). Less common or non-emerging TBDs in North America include such infections as babesiosis, which is caused by the protozoan Babesia microti and is transmitted by the blacklegged tick, primarily in southern New England and mid-Atlantic coastal areas (Spielman, 1976; Spielman et al., 1979). Powassan encephalitis is a rarely reported viral disease related to European TBE (Ebel, Spielman & Telford, 2001). Colorado tick fever (CTF) is a viral disease transmitted by the Rocky Mountain wood tick in the Rocky Mountain region (McLean et al., 1981). The lone star tick transmits Ehrlichia ewingi, which causes human ehrlichiosis. Q fever, caused by Coxiella burnetii, is primarily a livestock disease (McQuiston & Childs, 2002). Tick-borne relapsing fever, caused by several Borrelia spp. and transmitted by associated Ornithodoros spp., is primarily contracted by people in intermittently used recreational cabins in wild areas in western North America. Important vectors include Ornithodoros hermsi (which transmits the spirochete Borrelia hermsii), Ornithodoros parkeri (which transmits Borrelia parkerii), and Ornithodoros turicata (which transmits Borrelia turicatae) (Barbour, 2005). Tularaemia, caused by the bacterium Francisella tularensis, is usually acquired by rabbit hunters that handle infected rabbits (especially in eastern North America), but is sometimes transmitted by ticks (especially in western states). The following sections provide more comprehensive treatments of the most prevalent TBDs in Europe and North America: LB on both continents, TBE in Europe, and RMSF in North America. 10.4. Lyme borreliosis The clinical features, diagnosis, treatment, pathology, microbiology, ecology, surveillance and management of LB have been extensively reviewed (Ginsberg, 1993; Gray et al., 2002; Piesman & Gern, 2004; Steere, Coburn & Glickstein, 2005). Features relevant to current trends in LB epidemiology in Europe and North America are summarized below. 10.4.1. Public health LB is the most common TBD in both North America and northern Eurasia. The complex of related pathogenic species, B. burgdorferi s.l., the causative agents of LB, are Gramnegative, microaerophilic bacteria that belong to the family Spirochaetaceae. To date B. burgdorferi s.l. can be divided into at least 12 species (Fingerle et al., 2005), of which those with human-pathogenic significance are Borrelia afzelii, Borrelia burgdorferi sensu stricto, B. garinii, and Borrelia spielmanii (Richter et al., 2006). B. valaisiana and Borrelia lusitaniae may also be pathogenic to people (Ryffel et al., 1999; Collares-Pereira et al., 2004), but firm evidence is currently lacking. B. burgdorferi s.l. infection can be subclinical or it can have a broad range of clinical presentations (Gern & Falco, 2000). Symptoms apparently depend on the Borrelia genospecies involved, the tissues affected, the duration of infection and individual human host factors, including genetic predisposition. There is considerable evidence that infection with different LB genospecies have different clinical outcomes (Gern & Falco, 2000; WHO Regional Office for Europe, 2004). Thus, B. burgdorferi s.s. is most often associated with arthritis, particularly in North America, where it is the only known cause of human LB; B. garinii is associated with neurological symptoms; and B. afzelii is associated with the chronic skin disease acrodermatitis chronica atrophicans (ACA). All four pathogenic B. burgdorferi s.l. genospecies, including B. spielmanii (formerly named A14S), have been isolated from erythema migrans (EM) lesions (Fingerle et al., 2005). There is evidence in Europe that EM occurs more frequently in B. afzelii infections than in those caused by B. garinii. Generally, clinical presentations can be divided into three stages (Gern & Falco, 2000; Steere, Coburn & Glickstein, 2005).
According to treatment guidelines, LB treatment involves different antibiotic regimens in varying concentrations, adapted to specific clinical manifestation (Wormser et al., 2000). Doxycycline is effective in early LB. Amoxicillin and penicillin are also still drugs of choice. Treatment of late-stage disseminated LB requires higher doses, often of ceftriaxone or cefuroxime, and sometimes longer treatment periods. A specific vaccine for people, based on outer surface protein A (OspA), was temporarily available in the United States, but was withdrawn by the manufacturer in 2002. Due to the heterogenicity of B. burgdorferi s.l. genospecies in Europe and Asia, an effective vaccine for Europe would most probably require a defined so-called cocktail of immunogenic outer surface proteins. 10.4.1.1. LB in Europe and North America LB is broadly distributed in the northern hemisphere (Fig. 10.1). The prevalence of LB varies considerably among European countries, with estimated average rates between 0.3 case per 100000 population in the United Kingdom and up to 130 cases per 100000 population in parts of Austria. LB tends to be focal, with defined hot spots within countries. In Germany, for example, the average incidence in the Oder-Spree region in the federal state of Brandenburg was estimated to be 89.3 cases per 100000 population in 2003. Within this area, the local incidence of LB varied from 16 cases per 100000 population in Erkner county to 311cases per 100000 population in Brieskow-Finkenheerd county (Talaska, 2005; Anonymous, 2005a). Therefore, mapping hot spots is an important tool for disease prevention. Over 23000 cases of LB were reported to the CDC in 2002 (Groseclose et al., 2004), and it has been estimated that this is a small fraction (roughly 10%) of the actual total number of cases in the United States. In one study in Connecticut (Meek et al., 1996), about 16% of diagnosed cases had been reported. Cases follow the geographic distribution of the Ixodes vectors (the black-legged tick and the western black-legged tick) (Fig. 10.2), with most cases in the north-eastern, mid-Atlantic and northern Midwest regions (within the range of the black-legged tick), and with some hot spots in California (western blacklegged tick) (Dennis et al., 1998; Dennis & Hayes, 2002). As in Europe, the distribution of LB tends to be highly focal, because of nonrandom distributions of tick vectors, reservoir hosts, appropriate habitat types and other ecological conditions. This focal pattern is illustrated by the distribution of cases in 1999, when the national incidence was 6.0 cases per 100 000 population (16273 cases). The number of cases in individual states varied dramatically, with a maximal incidence of 98.0 cases per 100000 population in Connecticut (Dennis & Hayes, 2002). The costs associated with LB can be significant. Assuming a cost of about €10000 per case of so-called disseminated LB in Europe and, on average, 20–30% disseminated LBs per notified clinical case, with 1800–2000 cases a year in the federal state Brandenburg, an economic impact of €1 million a year can be easily exceeded for that state alone (Talaska, 2003). An economic burden of several €100 million up to 1 billion a year is plausible for Europe. Similarly, in the United States, Meltzer, Dennis & Orloski (1999) estimated costs (including treatment and lost work) of US$ 161 for early LB with no sequelae (previous diseases or injuries), US$ 34 354 for disseminated cases with arthritic symptoms, US$ 61243 for neurological cases and US$ 6845 for cardiac cases. Assuming 83% of cases with effective early treatment, and 17% with disseminated disease (12% with arthritic symptoms, 4% with neurological disease and 1% with cardiac disease), the total of about 23000 reported cases a year results in about US$150 million in costs. If the number of cases reported is only about 10% of the total number of cases, the actual costs are in US$ billions. These very rough estimates refer primarily to costs of medical treatment. Expenses associated with family accommodations for patients, lost work time and the like would greatly increase these estimates. Zhang and colleagues (2006) used actual cost data to estimate the economic impact of LB (including treatment and loss of productivity) in the Eastern Shore area of Maryland. They estimated a national cost of about US$ 203 million for the 23 763 cases reported in 2002. Again, unreported cases (probably the vast majority of actual cases) would greatly inflate this estimate. Furthermore, the costs of prevention activities associated with LB (such as landscaping and pesticide applications) contribute further to the costs of this disease, including human, economic and environmental costs. 10.4.2. Geographical distribution The global distribution of human pathogenic B. burgdorferi s.l. genospecies includes parts of North America and most of Europe and extends eastward in Asia to Japan (Fig. 10.1 and 10.2). In Europe, LB has been reported throughout the continent (including the European parts of the Russian Federation), except for the northernmost areas of Scandinavia. Taking the limitations of seroprevalence studies into account, LB in Europe shows a gradient of increasing incidence from west to east, with the highest rates of incidence in central-eastern Europe. Simultaneously, LB shows a gradient of decreasing incidence from south to north in Scandinavia and north to south in the European Mediterranean and Balkan countries (Lindgren, Talleklint & Polfeldt, 2000; Faulde et al., 2002; WHO Regional Office for Europe, 2004). The incidence of LB is apparently also increasing eastward in Asia. Infection rates are highest in adult ticks and vary between 10% and 30% in Europe (5–10% in nymphs), reaching up to a 45% positivity rate in adult ticks in hot spots of LB in Germany and Croatia (Hubalek & Halouzka, 1998; Kimmig, Oehme & Backe, 1998; Golubic & Zember, 2001). In the foreseeable future, the incidence of TBDs, especially LB, seem likely to increase, partly due to man-made environmental changes. For example, some current approaches to urban planning can provide additional ecotopes suitable for castor-bean tick and taiga tick, Ixodes persulcatus, infestations (Kriz et al., 2004). In North America, suburbanization has produced extensive suburban and periurban areas that provide an interface between urban and sylvan environments – a so-called border effect. Property sizes in these areas tend to be larger than in urban areas and therefore allow ready access to tick habitats that border infested natural ecosystems. This border effect is more pronounced in North America than in Europe. However, the European landscape is beginning to change. Increasing suburbanization can potentially create conditions similar to those in North America, as recently shown in the federal state of Mecklenburg-Western Pomerania, Germany (Talaska, 2003), potentially leading to greater human exposure to TBDs. Thus, the increase of LB is apparently related to that of urban sprawl, which often results in invasion of residential areas by deer and mice, providing reservoirs, tick hosts, and carriers for the spirochete (Matuschka et al., 1996). Moreover, some studies suggest that climate changes in Europe have resulted in a northern shift in the distributional limit of castor-bean ticks, an increase in their population density in Sweden and a shift into higher altitudes in mountainous areas in the Czech Republic (Lindgren, Talleklint & Polfeldt, 2000; Danielova, 2006). Castorbean tick nymphs infected with B. afzelii were found at altitudes up to 1024 m, and tick populations reached up to 1250–1270m. Thus, the range of LB is apparently increasing in Europe. The prevalence of ticks infected with B. burgdorferi s.l. has also increased at some sites (Kampen et al., 2004), possibly due to changes in climate or wildlife management. In the United States, LB is most common in the north-eastern and mid-Atlantic states and in the northern Midwest, with scattered foci in the south-eastern states and in California (Fig. 10.2). Scattered foci also exist in the Great Lakes region in southern Ontario and possibly other parts of Canada (Barker & Lindsay, 2000). Borrelia burgdorferi s.l. has been present in North America at least since the 1800s (Marshall et al., 1994). The increase and expanding range of LB in North America apparently results from a combination of factors: increasing populations of white-tailed deer (Odocoileus virginianus), an important host for adult black-legged ticks; habitat modifications that favour dissected second-growth woodlands (following movement of eastern farmers to the Midwest); and suburbanization that has produced excellent tick habitats and brought residents close to ticks (Spielman, Telford & Pollack, 1993). Genetic evidence suggests recent expansion of black-legged tick and B. burgdorferi populations in the north-eastern United States (Qiu et al., 2002). Borrelia burgdorferi s.s. is a generalist in the north-east, with individual genotypes infecting a variety of mammalian hosts, which may have contributed to its rapid expansion (Hanincová et al., 2006). Its range continues to expand – for example, with the spread of tick populations and LB cases in New Jersey and up the Hudson Valley of New York (White et al., 1991; Schulze, Jordan & Hung, 1998). 10.4.3. Epizootiology and epidemiology LB is a sylvatic zoonosis. Ticks that are generally associated with temperate deciduous woodlands that include patches of dense vegetation with little air movement and high humidity carry the infective agent. LB is also associated with some coniferous forests, when conditions are suitable for the ixodid tick vectors (Ginsberg et al., 2004). In open habitats in Europe, such as meadows and moorland, the main source of blood-meals is usually livestock, such as sheep and cows. With increasing frequency, ticks also occur in domestic settings when a moist microhabitat is provided by high grass, gardens and rough forest edges. Foliage, decomposing organic matter and litter can give shelter to both ticks and small mammals that act as hosts for immature ticks. Therefore, contemporary trends of suburbanization can potentially increase exposure in the peridomestic environment. Vector ticks are frequently encountered in residential areas (Maupin et al., 1991), and they are also encountered by people recreationally or occupationally exposed to forest habitats (Ginsberg & Ewing, 1989; Rath et al., 1996). Closed enzootic cycles that involve reservoir-competent hosts and host-specific ticks also have a role in maintaining LB in nature, and the spirochete can be transmitted to people when a bridge vector, such as the castor-bean tick, intrudes into the cycle. An example of this in Europe is the circulation of borreliae between the European hedgehog (Erinaceus europaeus) and the hedgehog tick, Ixodes hexagonus (Gern & Falco, 2000). Since the castorbean tick frequently feeds on hedgehogs, the potential is there for the hedgehog tick/hedgehog cycle to have a considerable impact on the eco-epidemiology (the specific association between an ecosystem or habitat and the enzootic transmission chain of reservoir hosts and vectors living therein) of LB in some areas. The widespread recommendation to encourage hedgehogs to live in home gardens, by preparing piles of leaf litter, may therefore contribute to the currently seen so-called urbanization cycle. Also, urban sprawl and invasion of commensal and non-commensal rodents can influence LB epidemiology. Norway rats, Rattus norwegicus, and garden dormice, Eliomys quercinus, can carry vector ticks and borreliae and can contribute to the urbanization of LB (Matuschka et al., 1996; Richter et al., 2004). In Europe, the castor-bean tick and the taiga tick serve as vectors to people, while the hedgehog tick transmits spirochetes among medium-sized mammals, and the seabird tick, Ixodes uriae, transmits B. garinii among seabirds. The prevalence of infection in nymphal sheep ticks averages 10.8% in Europe, with considerable variation among locales (Hubálek & Halouzka, 1998). In North America, the black-legged tick and western black-legged tick act as vectors to people, while Ixodes dentatus, Ixodes spinipalpus and other species serve as enzootic vectors to small animals, such as rabbits and wood rats (Eisen & Lane, 2002). The prevalence of infection in nymphal black-legged ticks varies from about 15% to 30% in endemic areas of the north-east (Piesman, 2002). A variety of other tick species, as well as some haematophagous insects, have been found to carry borreliae, but are most probably not involved in disease transmission. B. burgdorferi s.l. is transmitted transstadially by vector ticks, but transovarial transmission, while it occurs, is relatively rare. Besides these tick-specific transmission modes, a co-feeding effect has been described, in which uninfected ticks can acquire spirochetes while feeding near infected ticks on an uninfected host (Ogden, Nuttall & Randolph, 1997). Compared with North America, important differences in the ecology of LB in Europe result from the greater diversity of Borrelia spp. that cause human disease in Europe. Table 10.6 provides an overview of known genospecies of B. burgdorferi s.l., their primary vectors and reservoir hosts, geographical distribution, and virulence in people. In North America, B. burgdorferi s.s. is responsible for the vast majority of human cases, while in Europe, B. afzelii, B. garinii and B. valaisiana are most common. The most important reservoir in North America is the white-footed mouse, Peromyscus leucopus (Mather et al., 1989), and other rodents can also serve as major reservoirs, including voles (such as the meadow vole, Microtus pennsylvanicus), chipmunks (such as the eastern chipmunk, Tamias striatus) and rats (such as the Norway rat) (Smith et al., 1993; Markowski et al., 1998). Some North American birds, such as the American robin and the song sparrow, Melospiza melodia, can also serve as reservoirs (Richter et al., 2000; Ginsberg et al., 2005). In Europe, on the other hand, different species of Borrelia are associated with different wild hosts. The primary reservoirs of B. afzelii are rodents, including mice (Apodemus spp.) and voles (Clethrionomys spp.) (Kurtenbach et al., 2002a; Hanincová et al., 2003a). In contrast, the primary reservoirs of B. garinii and B. valaisiana are birds, including pheasants and songbirds (Humair et al., 1998; Kurtenbach et al., 1998, 2002b; Hanincová et al., 2003b). Reservoir competence varies among hosts. Lagomorphs, such as hares (Lepus spp.) and rabbits (Oryctolagus spp. and Sylvilagus spp.), show varying degrees of reservoir capacity. Similarly, carnivorous mammals, such as foxes (the red fox, Vulpes vulpes, for example), dogs (the domestic dog, Canis familiaris, for example) and cats (the domestic cat, Felis domesticus, for example), vary considerably in competence as reservoirs. Borreliae, however, are eliminated in ticks attached to some lizard species (Lane & Quistad, 1998), which apparently limits the importance of LB in areas where ground-dwelling lizards are abundant, such as south-eastern North America. In addition to their roles as reservoirs of some borreliae, many birds can serve as carriers of attached infected ticks when migrating (see Chapter 8). Ungulates (such as deer, sheep, cattle, goats and pigs) feed large numbers of mainly adult ticks in nature and may influence the epidemiology of LB, by increasing tick numbers (and thus the number of ticks per individual reservoir host), even if they themselves are not competent reservoirs. 10.5. TBE 10.5.1. Public health TBE is caused by the TBE virus (TBEV), a member of the RNA virus family Flaviviridae. Three subtypes can be differentiated. One of them causes central European encephalitis (CEE); this virus subtype was first isolated in 1937, and the castor-bean tick is the main vector. The Siberian and far-eastern subtypes (endemic in eastern Europe and throughout northern Asia) are the causative agents of Russian spring-summer encephalitis (RSSE), which is responsible for a disease similar to CEE, but with a more severe clinical course. The primary vector of RSSE is the taiga tick. Transmission can also occur on an epidemic scale after consumption of raw milk from TBE-infected goats, sheep or cows. Person-to-person transmission has not been reported. However, vertical virus transmission from an infected mother to her fœtus has been described (Hubálek & Halouzka, 1996). The incubation period of TBE is usually between 7 and 14 days (sometimes shorter with milk-borne transmission). A characteristic biphasic febrile illness occurs in about 30% of cases, with an initial phase that lasts 2–4 days, which corresponds to the viraemic phase. Symptoms are nonspecific and may include fever, malaise, anorexia, headache, muscle aches and nausea or vomiting (or both). After a remission phase of about 8 days, up to 25% of the patients develop an infection of the central nervous system with symptoms of meningitis (50%), encephalitis or meningoencephalitis (40%) and myelitis (10%). Case fatality rates are generally below 5% in European TBE, but they are up to 50% in some outbreaks of Asian subtypes (Nuttall & Labuda, 2005). In up to 40% of cases, convalescence can be prolonged by sequelae (known as post-encephalitic syndrome), and about 4% of the CEE cases produce a residual paresis (slight or partial motor paralysis). Treatment depends on the symptoms and often requires hospitalization and intensive care. Anti-inflammatory drugs are sometimes utilized, and intubation and ventilatory support are sometimes necessary. Licensed vaccines (active and passive) that neutralize all three virus subtypes (Rendi-Wagner, 2005) are commercially available, with protection rates exceeding 98%. 10.5.1.1. Public health impact of TBE in Europe TBE is the most frequent viral TBD in central Europe. Overall, several thousand clinical cases a year occur in Europe: mainly in the Russian Federation (5000–7000 cases a year), the Czech Republic (400–800 cases a year), Latvia (400–800 cases a year), Lithuania (100–400 cases a year), Slovenia (200–300 cases a year), Germany (200–400 cases a year) and Hungary (50–250 cases a year). In 1997, 10208 clinical cases of TBE (with 121 fatalities) were reported from all over Europe. In 2005, a sharp increase of 50% or more in notified clinical cases of TBE was seen in Switzerland (91 cases in 2004 versus 141 cases in 2005; weeks 1–33) (Anonymous, 2005b) and Germany (258 cases in 2004 versus 426 cases in 2005) (Anonymous, 2005b). Since treatment of this potentially fatal disease depends on the symptoms, vaccination, prevention of infective tick-bite and pasteurization of contaminated milk constitute the first line of defense in preventing TBE. Due to the frequent need for hospitalization (often with intensive care), subsequent prolonged recovery time and neurotropic sequelae, the economic impact of this disease, in addition to its effect on health, is costly. As has been reported in Austria, vaccination programmes can substantially lower the annual incidence of TBE. Vaccination coverage of the Austrian population increased from 6% in 1980 to 86% in 2001, exceeding 90% in some hyperendemic areas (Kunz, 2003). This programme led to a steady decline in cases of TBE, drastically reducing the annual health impact for Austria to less than 10%. For example, in Carinthia, Austria, there were an average of 155 cases a year from 1973 to 1982, while from 1997 to 2001 there were only four cases a year (Kunz, 2003). In Hungary, 3–5% of the population were reported to be vaccinated, and in the southern Bohemia region of the Czech Republic it was 10% (WHO Regional Office for Europe, 2004). For other European countries, the vaccination status is unknown, but is probably low (Kunz, 2003). 10.5.2. Geographical distribution The currently known geographical distribution of European TBE foci includes much of central and eastern Europe and extends broadly into Asia. Randolph (2001) predicted an eventual future decline in the distribution and incidence of TBE, due to global climate change, but currently both the geographical distribution and incidence of infection are increasing. Therefore, programmes that promote vaccination and prevention of tick bites are essential in highly affected areas. TBE has recently spread in a north-westerly direction from central Europe to western Germany and has moved north to Finland, Norway and Sweden, as well as to higher altitudes in mountainous areas in the Czech Republic (Hillyard, 1996). The north-westward spread of TBE might be explained by:
Milder winter temperatures in particular have important effects on tick distribution and can foster shifts into higher latitudes and altitudes (Lindgren, Talleklint & Polfeldt, 2000). 10.5.3. Epizootiology and epidemiology Ixodid ticks act as both the vector and reservoir for TBEV. This virus can chronically infect ticks and can be transmitted transstadially and transovarially. Small rodents are the main hosts, although viraemia has been reported from insectivores (representing an order of mammals whose members basically feed on insects and other arthropods), goats, sheep, cattle, canids (which include foxes, wolves, dogs, jackals and coyotes) and birds. People are an accidental host, and large mammals are feeding hosts for adult vector ticks, but do not play a significant role in maintaining the natural virus cycle. The infection rates in castor-bean ticks and taiga ticks in endemic foci usually vary from 0.1% to 5%, but can reach up to 10% in hyperendemic foci – for example, in Austria. The rate of infection increases steadily from the larval to the adult stage. Human TBE cases occur mainly during the highest period of vector tick activity, between April and November, peaking from mid-June to early August. Nevertheless, sheep ticks can be active at any temperatures above about 10°C, even during winter. Thus sporadic clinical cases occur even during wintertime. TBE is usually contracted in habitats suitable for the vector tick species and primary rodent reservoirs. These include mixed forest, pastoral and mountainous sylvan areas for castor-bean ticks and mixed taiga forest for taiga ticks. During recent years, man-made changes in natural areas have increased the periurban abundance of both tick species. This trend is associated with growing disease transmission, including a tendency towards urban transmission. Urban TBE transmission has been described in Europe and Asia – for example, in Novosibirsk, the Russian Federation (Hubalek & Halouzka, 1996). Commensal rodents, cats and dogs are known to carry host-seeking ticks into human dwellings in periurban and urban areas. Ixodes ticks can survive for several hours and bite humans, but they do not persist in houses or stables. TBE is most likely to be acquired in forests rich in small mammals, so forest workers, hunters and others highly exposed to this ecotope are at high risk. The seroprevalence of this virus in foresters can reach 12–16% in hyperendemic foci – for example, in Austria and Switzerland. In Germany, seroprevalence rates exceeding 20% have been found in foresters in the Emmendingen and Ludwigsburg counties (Kimmig, Oehme & Backe, 1998). TBE morbidity rates in the Czech Republic and Slovakia averaged 4.2 (1.4–9.9) deaths per 100000 population between 1955 and 2000. In Switzerland (Thurgau canton) a morbidity rate of 5.4 people per 100000 population was estimated for 1995. The highest morbidity in Germany was estimated for the federal state of Baden-Württemberg, with 1.1 cases per 100000 population. In some cases, up to 76% of human TBE infections can result from consumption of raw milk, as was reported in Belarus (Ivanova, 1984). 10.6. RMSF 10.6.1. Public health RMSF was first recognized in an epidemic in the Bitterroot Valley of Montana, in the United States, in the late 1800s. The etiological agent is Rickettsia rickettsii, and the primary vectors are the American dog tick in eastern and central North America and the Rocky Mountain wood tick in the Rocky Mountain region (Sonenshine, Lane & Nicholson, 2002). The number of cases reported to the CDC varies from about 200 to about 1200 a year, with an average incidence from 1985 to 2002 of between 0.24 to 0.32 cases per 100000 population (Schriefer & Azad, 1994). RMSF is characterized by the sudden onset of high fever, headache and myalgia, often with nausea and other symptoms (Macaluso & Azad, 2005). A few days after the onset of symptoms, a rash generally appears, beginning as macropapular eruptions on the ankles and wrists that then spread to the entire body, producing a so-called spotted appearance. The rickettsiae are intracellular parasites that affect (in particular) cells of the capillaries and arterioles. Symptoms are often severe, and though early treatment (generally with tetracyclines) is effective, the disease is fatal in around 5% of cases. 10.6.2. Geographical distribution The distribution of human cases of RMSF, or at least the distribution of recognized cases, has shifted from the Rocky Mountain region in the late 1800s to eastern and central North America today. The incidence of the disease is currently highest in the south-eastern and south-central states (such as the Carolinas and Oklahoma), but cases are scattered throughout the eastern and central regions of North America (Fig. 10.3), with relatively few cases in the Rocky Mountain and western states (Groseclose et al. 2004; Macaluso & Azad, 2005). 10.6.3. Epizootiology and epidemiology RMSF is generally acquired in rural and suburban areas with woodland and associated open vegetation where the tick vectors are abundant (Sonenshine, Peters & Levy, 1972; Sonenshine, Lane & Nicholson, 2002). However, foci sometimes occur in appropriate habitats within large cities (Salgo et al., 1988). The pathogen is transmitted vertically in the tick (from mother to offspring) and is maintained transstadially, so the tick can act as both vector and reservoir. However, infection with nonpathogenic rickettsiae can interfere with transovarial transmission (Burgdorfer, Hayes & Mavros, 1981). Small mammals also can serve as reservoirs and apparently can contribute to amplification under appropriate circumstances, but occurrence of RMSF does not seem to depend on any particular vertebrate reservoir (Schriefer & Azad, 1994). Larvae and nymphs of American dog ticks and Rocky Mountain wood ticks attach to a variety of small and medium-sized mammals, including mice, voles, rats, ground squirrels, hares and rabbits, many of which can maintain infection with spotted fever group rickettsiae. Adults of these tick species generally attach to larger mammals, including human beings. Infection rates of adults vary considerably from site to site, ranging from less than 1% to about 10%. 10.7. Emerging TBDs Several TBDs have recently been recognized in Europe and North America. Some of these might represent new introductions of the diseases to these continents, while others were undoubtedly already present, but were recognized recently because of the renewed attention to TBDs that resulted from the recent increase of LB. Also, some diseases that have been rare in the past are apparently expanding in range, along with expanding tick populations. Selected diseases that have recently been recognized in North America and Europe are discussed in this section. 10.7.1. Crimean-Congo haemorrhagic fever Crimean-Congo haemorrhagic fever (CCHF) was first mentioned by the Tajik physician Abu-Ibrahim Djurdjani in the 12th century and has been extensively studied since the 1944/1945 epidemic in the Crimean Peninsula (Hubalek & Halouzka, 1996). This epidemic resulted in more than 200 human cases, with 10% of them fatal. The disease is caused by the CCHF virus (CCHFV), a Nairovirus (family Bunyaviridae) closely related to Dugbe and Nairobi sheep disease viruses and classified as a biosafety level-4 virus (the highest biological security level). The clinical course appears as a haemorrhagic fever with severe typhoid-like symptoms, including fever, chills, headache, myalgia, backache, anorexia, nausea, repeated vomiting, conjunctivitis, pharyngitis, bradycardia, meningitis and encephalitis. Haemorrhagic manifestations can vary from petechiae (pinpoint-sized haemorrhages of small capillaries in the skin) to large haematomas (solid swellings of clotted blood within tissues) on the mucous membranes and skin, and bleeding from the gums, nose and intestines and, less frequently, lungs and kidneys. Case fatality rates are usually between 8% and 30%, but may reach up to 50–60% in cases transmitted from person to person (Hubalek & Halouzka, 1996). Convalescence is slow, but usually without sequelae. Treatment of confirmed human cases requires barrier nursing and special hygienic care to prevent nosocomial infection. Treatment usually depends on the symptoms, but treatment with ribavirin seems promising during the early stages of the disease (Ozkurt et al., 2006). An inactivated CCHF vaccine was administered to several hundred people in Bulgaria and Ukraine (Rostov oblast), but severe side-effects appeared. Specific immunoglobulins can also be used prophylactically or therapeutically. However, no licensed, safe vaccine is currently available. CCHF is the most severe TBD in Europe and has the potential to spread quickly from person to person. The disease is probably underreported worldwide, so European and global incidences are unknown. Bulgaria, the southern part of the Russian Federation and Ukraine are among the most highly affected areas within Europe. Cases have also been reported from Bosnia and Herzegovina, Greece, Hungary, Montenegro, the Republic of Moldova, Serbia, and the former Yugoslav Republic of Macedonia. From 1952 to 1970, 865 cases of CCHF were recorded in Bulgaria alone, with a case fatality rate of 17%, and 6% of the cases of nosocomial origin (Vasilenko et al., 1971). In the Rostov region, 312 cases were registered between 1963 and 1969. Human cases sporadically occur in that region, with an outbreak occurring in 1999 (65 cases with 6 fatalities) (Onishchenko et al., 2000). The virus has been detected in almost all south-eastern districts of the Russian Federation, resulting in an additional regional budget of Rub 2.5 million (US$ 872000) for diagnostic procedures and preventive measures (ProMED Mail, 2005). In 2002, eight cases clustered within families were observed in Albania (Papa et al., 2002). Although the overall incidence for Europe remains unclear, CCHF is a reemerging disease with an estimated annual incidence far greater than100 cases, especially during outbreaks (Faulde et al., 2002). The bont-legged tick, Hyalomma marginatum, is the principal vector and tick reservoir of CCHFV in Europe. Transstadial, transovarial and venereal transmission occur. This tick species inhabits pastoral steppe ecosystems, and the adult stage frequently feeds on sheep. CCHFV is highly contagious and transmission to people can occur by tick bite, by contact with infected animals (such as during sheep shearing and meat handling) and by person-to-person contact. Laboratory infections have also been reported. 10.7.2. Tick-borne rickettsioses Several new human-pathogenic tick-borne rickettsioses of the spotted fever group have been reported from Europe during the last decade. Among them, Rickettsia conorii and Rickettsia helvetica are of greatest concern. Rickettsia slovaca, Rickettsia aeschlimannii and Rickettsia mongolotimonae are also endemic, although with very few human cases reported to date. Novel rickettsioses have recently been described in North America as well. 10.7.2.1. Boutonneuse fever R. conorii is the causative agent of Boutonneuse fever (BF), also known as tick-borne typhus, Mediterranean spotted fever and South African tick bite fever. Patients usually present with fever, malaise, a generalized maculopapular erythematous rash and a typical black skin lesion, called tache noir, at the site of the infected-tick bite. While the disease is usually mild, severe forms, including encephalitis, occur occasionally. Overall, the case fatality rate in Europe is estimated to be less than 2.5%, even if untreated. Fever usually persists for a few days to two weeks, with a specific antibiotic treatment required for no more than two days. The seroprevalence rates in dogs, which are often infested with up to 100 adult brown dog ticks per animal, can be quite high in hyperendemic foci, varying between 35.5% in Italy and 93.3% in Portugal. The annual incidence rate in people has been estimated to be 48 cases per 100 000 population in Corsica, France, whereas 1000 cases have been reported annually from Portugal. Human seroprevalence rates can exceed 70% in hyperendemic foci in Spain (WHO Regional Office for Europe, 2004). However, the overall incidence of BF in Europe is unclear. R. conorii is widely found in southern Europe and the Mediterranean countries. This disease is spreading northwards, reaching Belgium, Germany and the Netherlands, where antibodies were detected in dogs and people, and R. conorii has been isolated from sheep ticks and rodents in Belgium (Jardin, Giroud & LeRay, 1969; Gothe, 1999; WHO Regional Office for Europe, 2004). The major tick vector of R. conorii in Europe is the brown dog tick. Other vectors include the castor-bean tick, the hedgehog tick, the marsh tick (also called the ornate cow tick), Dermacentor reticulatus, and the ornate sheep tick, Dermacentor marginatus. Besides vector ticks, the primary reservoirs are dogs, rabbits and rodents. Pet dogs can acquire infected ticks during family holidays, and they can carry R. conorii with them when they return home further north in Europe. Human infection with BF in urban areas, often in a person’s own home, can be caused by skin or eye contamination from rickettsiae-infected dog ticks that are crushed while de-ticking infested dogs (Hillyard, 1996). 10.7.2.2. Rickettsia helvetica First isolated in Switzerland in 1979, this agent was linked with human disease in 1999, when it was associated with two fatal Swedish cases of chronic perimyocarditis (Nilsson, Lindquist & Pahlson, 1999). R. helvetica is now known to have caused chronic interstitial inflammation and pericarditis in people in France, Sweden and Switzerland. A serosurvey of foresters conducted after seroconversion of a 37-year-old man in 1997 in eastern France revealed a seroprevalence rate of 9.2% (Fournier et al., 2000). The disease is transmitted by the castor-bean tick, and initial results show infection rates in ticks between 1.7% in Sweden and 8.2% in northern and central Italy (Nilsson et al., 1999; Beninati et al., 2002). Recent studies indicate that R. helvetica is widely distributed throughout Europe and might cause more clinical disease and (even) mortality than is currently recognized (WHO Regional Office for Europe, 2004). 10.7.2.3. HME HME is caused by the rickettsial pathogen Ehrlichia chaffeensis. In North America, this pathogen exists in a tick–deer cycle, with the lone star tick serving as the primary vector (Ewing et al., 1995) and the white-tailed deer serving as the primary reservoir (Lockhart et al., 1997). Human cases are most common in the southern Midwest, with foci along the East Coast (Dawson et al., 2005). In 2001, 142 cases were reported in the United States; in 2002, 216 cases were reported; and in 2003, 321 cases were reported (CDC, 2003; Groseclose et al., 2004; Hopkins et al., 2005). E. chaffeensis has also been found to be endemic in Europe – in Belgium, the Czech Republic, Denmark, Greece, Italy and Sweden – but human cases of disease have not been described to date (WHO Regional Office for Europe, 2004; Oteo & Brouqui, 2005). 10.7.2.4. HGA HGA is caused by the rickettsial pathogen Anaplasma phagocytophilum (formerly Ehrlichia phagocytophila). Patients present with an acute febrile illness, and most develop leukopenia or thrombocytopenia (or both), and elevated concentrations of C-reactive protein and transaminases, with occasional fatalities occurring. Treatment with tetracycline generally leads to full recovery. The pathogen was first isolated from ticks and people in northern Midwestern United States in the 1990s (Chen et al., 1994; Dumler et al., 2001). The black-legged tick is the vector in the United States, and its mammal hosts, especially the white-footed mouse, serve as reservoirs (Pancholi et al., 1995; Levin & Fish, 2001). The United States distribution includes the Atlantic coastal states, the northern Midwest and California (CDC, 2003; Maurin, Bakken & Dummler, 2003; Brown, Lane & Dennis, 2005). In 2001, 261 cases were reported to the CDC; in 2002, 511 cases were reported (CDC, 2003; Groseclose et al., 2004). In Europe, HGA in people was first recognized in 1995, when serum antibodies against A. phagocytophilum were confirmed. In 1997, the first proven European case of human disease was reported from Slovenia. Through March 2003, about 65 patients with confirmed HGA (and several patients fulfilling criteria for probable HGA) had been reported in Europe (Strle, 2004). Seroprevalence rates in the WHO European Region range from 0% to 28%, and infection rates in adult castor-bean ticks (the recognized tick vector) range from 0% to more than 30%. The relatively high seroprevalence rates in people and the presence of A. phagocytophilum in vector ticks in many European countries are discordant with the rather low number of patients with proven HGA. This may be due to an inadequate awareness among European physicians and limited recording and reporting of the disease, or it may be due to the presence of nonpathogenic strains of A. phagocytophilum (Strle, 2004). The castor-bean tick is probably the principal vector in Europe and the taiga tick in north-eastern Europe and Asia, although transmission studies have not been reported to date. HGA is known to cause febrile illness in several domestic animals, including sheep, goats, cattle and horses. A Swiss study stressed the importance of small mammals, with the bank vole, Clethrionomys glareolus, wood mouse, Apodemus sylvaticus, yellow-necked mouse, Apodemus flavicollis, and common shrew, Sorex araneus, as likely animal reservoirs in nature (Liz, 2002). 10.7.3. Babesiosis Human babesiosis, first described in 1957, is a malaria-like illness caused by piroplasms (pear-shaped protozoan organisms that live in red blood cells of mammals), including B. microti in North America and Babesia divergens in Europe (Homer & Persing, 2005). The primary vectors are the black-legged tick in eastern North America and the castor-bean tick in Europe. Rodents, such as white-footed mice serve as reservoirs (Spielman, 1976; Spielman et al., 1979). Babesiosis is often mild and self-limiting, but can be severe and is undoubtedly underreported. Nevertheless, hundreds of cases have been reported in North America, and 29 in Europe (from England and France). In the United States, cases have been reported primarily in coastal areas of the north-eastern and mid-Atlantic states (Dammin et al., 1981; Spielman et al., 1985). 10.8. Ticks in human dwellings In Europe, the brown dog tick can persist in long-term infestations of human dwellings with dogs. The European pigeon tick can also occur in dwellings with pigeon infestations or breeding. The fowl tick and Ornithodoros erraticus may also occur in houses close to poultry stables (Argas spp.) in south-east Europe and pig stables (Ornithodoros spp.) in Spain and Portugal. Ticks found in human dwellings in North America are primarily soft ticks (of the genus Ornithodoros) associated with rodents that nest in buildings. The most important human disease transmitted by these ticks is tick-borne relapsing fever, which is caused by various species of the bacterial genus Borrelia. The most common pathogens in this group are B. hermsi (transmitted by O. hermsi) in mountainous areas of the western United States and Canada, and B. turicatae (transmitted by O. turicata) in desert and scrub habitats in the south-western United States and Mexico (Barbour, 2005). People generally encounter these pathogens recreationally, when occupying rustic cabins that are inhabited by tickbearing rodents. Recently, specimens of the bat-associated soft tick, Carios kelleyi (collected from buildings in Iowa) were found to be infected with spotted fever group Rickettsia, relapsing fever group Borrelia, and Bartonella henselae (the etiological agent of cat scratch disease), but the role of these ticks as vectors of these bacterial pathogens has not been established (Loftis et al., 2005). Also, the brown dog tick can be found in homes, associated with dogs, but generally does not bite people. 10.9. Tick and tick-borne disease surveillance TBDs that are reportable in the United States include LB, RMSF, HME, HGA, Q fever, and tularaemia (Hopkins et al. 2005). In Europe, where regulations differ among countries, only TBE is widely reportable. Active surveillance for ticks or TBDs requires purposeful sampling of ticks or samples from wild or domestic hosts, or from people (Nicholson & Mather, 1996; Lindenmayer, Marshall & Onderdonk, 1991). Passive surveillance, on the other hand, utilizes information collected for other purposes, such as data collected from tick laboratories or hospital registries, to assess tick or disease distribution (White, 1993). Active surveillance tends to provide more accurate information, but is expensive and labour intensive. Passive surveillance is less expensive and requires less effort, and it can provide useful information of appropriate types, but the value of the results are sometimes limited by unidentifiable biases in data collection (Johnson et al., 2004). Most current tick surveillance programmes are of the passive type. 10.10. Tick and TBD management Ticks are controlled for a variety of reasons, including nuisance prevention, commodity protection (to prevent cattle loss, for example) and protection against TBDs. This section briefly reviews tick control methods and then discusses IPM strategies that are appropriate for various purposes of tick control. 10.10.1. Self-protection 10.10.1.1. Avoidance Ticks can be avoided by refraining from exposure to fields, forests and other hard tickinfested habitats, especially in known disease foci (Ginsberg & Stafford, 2005). Specific habitats to be avoided depend on tick distribution, which can differ for different species and for different stages of the same species. Use of clearly defined paths can help avoid contact with tick-infested vegetation. Bites of soft ticks can be prevented by avoiding old campsites, animal and poultry stables, and infested cabins and mud houses and by taking appropriate precautions when coming in contact with animals that are potentially infested with ticks. 10.10.1.2. Repellents Effective repellents can prevent ticks from becoming attached to the body and can be applied to clothing or directly on the skin (some products are not labelled for use on skin). Effective skin repellents include N,N-diethyl-3-methylbenzamide (DEET), (N,N-butylN-acetyl)-aminopropionic acid-ethyl ester and 1-piperidinecarboxylic acid 2-(2-hydroxyethyl)-1-methylpropylester (picaridin). Depending on the active ingredient and formulation, skin repellents generally do not last longer than a few hours, because of absorption or abrasion. 10.10.1.3. Clothing Individuals can protect themselves against tick attachment by tucking trousers into boots or socks and tucking shirts into trousers. Light-coloured clothing aids detection of darkcoloured ticks, which can be collected or removed with commercial tape. Most TBDs require a period of attachment (often several hours) before the pathogen is transmitted, so thorough body examination and prompt removal of attached ticks at the end of a day spent in tick-infested areas can minimize exposure to TBD agents. 10.10.1.4. Tick removal Hard ticks should be removed by grasping the tick where the mouthparts are attached to the skin and then pulling it out slowly, but steadily (Needham, 1985); the use of pointed forceps is preferable, because it avoids contact with fingers and the tick’s infective body fluid or excreta. The bite site should be cleansed with antiseptic before and after removal. Soft ticks withdraw their mouthparts when touched with a hot needle tip or when dabbed with chloroform, ether, alcohol or other anaesthetics (Gammons & Salam, 2002). 10.10.1.5. Clothing impregnation A major advance in the protection of high-risk personnel, such as outdoor workers, hunters, travellers and soldiers, has been the development of residual insecticides that can impregnate clothing, tents and netting (WHO, 2001a, b). Permethrin, a synthetic pyrethroid insecticide, has been widely used for decades as an arthropod contact repellent in fabric impregnation, by spraying or soaking the fabric at final concentrations between 500mg/m2 and 1,300mg/m2 (Young & Evans, 1998; Faulde, Uedelhoven & Robbins, 2003). Recently, factory-based impregnation methods have been introduced, such as soaking the fabric or using a new polymer-coating technique for impregnating clothing and battle dress uniforms. The polymer coating is safe, and the impregnation lasts the life of the fabric (Faulde & Uedelhoven, 2006). Ticks crawling up impregnated fabric quickly fall off. The benefits to people are the bites prevented and the acaricidal activity. This method can also be used to protect against other haematophagous arthropod vectors of public health importance. 10.10.1.6. Vaccination Of tick-borne diseases endemic in Europe and North America, only TBE can be prevented by the use of a vaccine. TBE vaccination is widely neglected as a public health tool for disease prevention (Austria is an exception). A vaccine for preventing LB was briefly available in North America, but this was specific to B. burgdorferi s.s. and would not be efficacious in Europe, where diverse Borrelia spp. are associated with LB in people. The manufacturer removed the vaccine from production in 2002, and no vaccine against LB is currently available. 10.10.2. Habitat manipulation and urban design Ticks have species-specific habitat requirements, often associated with habitats of hosts and the need to avoid desiccation. Therefore, habitats can be manipulated to make them unsuitable for ticks or to minimize encounters between ticks and people (Stafford, 2004). Suburban habitats associated with natural woodlands foster populations of black-legged ticks and castor-bean ticks, because these habitats are excellent for both immature and adult ticks and for vertebrate hosts suitable for all tick stages. Lawns that were cut short and were open to the sun had minimal numbers of deer ticks, while tick densities increased incrementally in gardens, wood edges and forests (Maupin et al., 1991). Therefore, maintaining a short-clipped lawn and establishing barriers to prevent access to the woods can minimize human exposure to ticks in this environment. Mowing and burning vegetation in natural areas lowers tick numbers temporarily, but ticks reinfest treated areas as the vegetation grows back (Wilson, 1986). Most ticks that are important to human health are rare in highly urbanized environments, but parks with natural patches and appropriate host species, and natural habitats interspersed with human dwellings in suburban areas, foster encounters between ticks and people. These encounters can be minimized with appropriate design features, such as barriers between areas frequently used by people and natural patches, and pathways constructed through natural sites (boardwalks, for example). Medical entomologists and natural resource experts should be consulted, so that urban design appropriate for the local tick species of concern can be incorporated into the planning process. Unfortunately, in the past, TBDs have rarely been considered in urban or suburban design. 10.10.3. Host-centred methods Domestic animals can be vaccinated to minimize tick attachment (de la Fuente, Rodriguez & Garcia-Garcia, 2000) or to protect them against TBDs (Kocan et al., 2001). House pets, especially dogs, are commonly vaccinated against LB in the United States. Vaccination of wild reservoir species of animals (Tsao et al., 2001) could theoretically interrupt enzootic transmission cycles of tick-borne zoonoses and, in field trials, it has reduced the prevalence of Lyme spirochetes in questing ticks (Tsao et al., 2004), but this approach has not yet been applied to manage the risk of disease. Manipulation of host populations can also lower tick populations. Excluding deer can lower populations of deer ticks, and deer-proof fencing can contribute to a tick management programme (Daniels, Fish & Schwartz, 1993). Although lowering deer populations by hunting can also lower tick numbers, this approach is not generally practical, because deer populations must be reduced to extremely low levels to have a reliable effect on the transmission of LB (Ginsberg & Stafford, 2005). 10.10.4. Biological control Ticks have numerous natural enemies, including predators, parasites and pathogens. In the northern hemisphere, predators are generally not specific to ticks. In contrast, wasps of the genus Ixodiphagus parasitize ticks, and the most widespread species, Ixodiphagus hookeri, has been studied as a possible biocontrol agent. This species was released on an island off the New England coast in the early 1900s, resulting in establishment of the wasp, but no tick control. Inundative releases have shown some promise of efficacy in agricultural settings (Mwangi et al., 1997), and theoretical analyses suggest that with additional research and development widespread releases might eventually be effective in North America (Knipling & Steelman, 2000). However, considerable problems remain to be overcome before this approach becomes practical. Numerous pathogens attack ticks, including bacteria, fungi, and nematodes (Samish, Ginsberg & Glazer, 2004). At present, one of the best candidates for tick biocontrol is the entomopathogenic fungus, Metarhizium anisopliae (Zhioua et al., 1997; Samish et al., 2001). Preliminary field trials have had modest results; but enhanced tick mortality, from the use of an oil-based carrier solution, compared with a water-based solution (Kaaya & Hassan, 2000), suggests that improved formulations may provide effective control. The pathogens that affect ticks typically also affect other arthropods (Ginsberg et al., 2002), so effects on non-target arthropods must be considered in application strategies of biocontrol materials. 10.10.5. Pesticide applications Numerous pesticides are effective against ticks, and they are widely used to control ticks and TBDs. Acaricides can be broadcast for area control of ticks or can be targeted at host animals used by the ticks. Broadcast applications have the advantage that they can rapidly lower tick numbers, but timing, chemical distribution and formulation can profoundly influence the effectiveness of treatment. For example, broadcast applications for controlling nymphal deer ticks (the primary vector stage of LB in North America) need to penetrate the leaf litter where the nymphs dwell, while other ticks are better targeted by area sprays. Schulze, Jordan & Hung (2000) found that granular formulations of carbaryl effectively controlled deer tick nymphs (which quest down in the leaf litter where the heavy granules were deposited), but they did not control lone star tick nymphs (which quest up in the shrub layer). Also, most materials used for tick control are broadly toxic to arthropods, so broadcast applications can have substantial effects on non-target species (Ginsberg, 1994). Pesticide applications that are carefully targeted can help minimize these non-target effects. Application concentrations for tick control vary with materials and formulations, but examples of label application concentrations include: carbaryl (43% by weight, 0.17–0.34g/m2); cyfluthrin (11.8% by weight, 0.04–0.065ml/m2); and permethrin (36.8% by weight, 0.12–0.24g/m2). Pesticides can be targeted at host animals by attracting the hosts (using feed, nesting materials or other attractants) to devices that apply the pesticide to them. Examples include bait boxes, permethrin-treated cotton balls and so-called four-poster devices (Stafford & Kitron, 2002). Four-poster devices, which coat the heads and necks of animals with a pesticide that kills the ticks, have the advantage of well-targeted applications, allowing far lower amounts of pesticide to be applied than in broadcast applications. The effectiveness of the approach taken tends to depend on ecological conditions at the application site. These methods can be important tools in IPM programmes, especially when integrated with other management techniques appropriate for local conditions of tick distribution and transmission dynamics. Permanent infestations in houses and stables – for example by the brown dog tick or the pigeon tick – require the professional use of acaricides. Governmental European authorities – for example, in Germany – recommend the use of formulations that contain popoxur (1% by weight, 200 ml/m2) and diazinon (2% by weight, 50–100 ml/m2) (Anonymous, 2000). Besides the application of acaricides, dog hosts have to be treated with tick-repelling or -controlling spot-on or dipping formulations, and construction modifications of infested houses and stables are needed to prevent further infestations of pigeons, which are natural hosts of pigeon ticks (Uspensky & Ioffe-Uspensky, 2002). 10.11. IPM IPM is an approach to the management of arthropod pests that fosters the integration of various pest control methods, so as to minimize reliance on individual environmentally damaging approaches and to provide sustained management of pest populations. IPM was developed for agriculture, where decisions are based on cost–benefit analyses that compare the cost of control with the economic value of crops protected. For vector-borne diseases, decisions are more appropriately based on cost–effectiveness (or cost–efficiency) analyses that integrate management methods, so as to prevent the greatest number of possible human cases of disease at a given cost (Phillips, Mills & Dye, 1993; Ginsberg & Stafford, 2005). Efficient management of TBDs maximizes the number of human cases prevented with available resources and minimizes dependence on broad-spectrum approaches to control that tend to be environmentally damaging. However, these analyses require information from field trials of various management methods and from models of transmission dynamics that use each potential combination of techniques to estimate the costs and the number of cases prevented (Mount, Haile & Daniels, 1997). Given the many tick control techniques currently available and the numerous novel techniques being developed, it is important to develop the theory and practice of efficient integration of methods, so that these techniques can be applied in such a manner as to most effectively prevent human disease. 10.12. Conclusions The following conclusions can be drawn about public activities, surveillance and management, and research. 10.12.1. Public activities Conclusions that relate to public activities cover three areas, as follows.
10.12.2. Surveillance and management Conclusions that relate to surveillance and management cover two areas, as follows.
10.12.3. Research Conclusions that relate to research cover three main areas, as follows.
Followed by references |