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Check out the new and updated website of the National Alliance of Safe Pest Control: http://www.pests.org The world tick fauna comprises about 900 species of which New Zealand has 11 confirmed.1 Four of these are endemic (kiwi tick, Ixodes anatis; tuatara tick, Amblyomma (formerly Aponomma)sphenodonti and the cormorant tick, I. jacksoni), as well as a new species of Carios from a native bat, and the others are either exotic (Carios (formerly Ornithodoros) capensis, Haemaphysalis longicornis, Ixodes amersoni ) or shared with Australia (Ixodes eudyptidis), or distributed throughout the sub-Antarctic faunal region (I. kerguelenensis, I. auritulus zealandicus, and I. uriae). OnlyH. longicornis has been recorded from humans in New Zealand, with C. capensis capable but not reported doing so in this country. Figure 1. Engorged female New Zealand cattle tick, Haemaphysalis longicornis (left); and (right) male (small tick) and engorged female paralysis ticks, Ixodes holocyclus (photos courtesy of Wikipedia under the Creative Commons Attribution-Share Alike 3.0 Unported license) Ticks are of considerable economic importance as far as livestock are concerned2 and stringent measures are employed to keep these exotic parasites out of New Zealand. Companion and other live animals imported into New Zealand are subject to import health standards that comprise pre-export treatment with an acaricide, as well as veterinary inspection and clearance. Companion animal imports from countries where rabies is endemic are also subject to quarantine.3 Humans are not subject to such measures but worldwide, are an important pathway for exotic ticks.4 By travelling extensively, New Zealanders increase their risk of being infested by ticks and catching tick-borne disease. First we outline the biology, ecology and diseases associated with ticks and then we review details of all instances that we could find of exotic ticks found on travellers that had entered New Zealand, or which were associated with their belongings or activities, both to draw the attention of the medical profession to the magnitude of this problem, and to raise awareness of the risks posed to public health. The vector potential of ticks that occur in New Zealand is also discussed. Tick biology Ticks are arthropods that require blood to survive and reproduce. This characteristic and their often remarkable longevity make them ideal candidates for the transmission of many types of disease organisms. In addition, ticks can also cause a variety of medical conditions ranging from localised irritation to anaemia and, with some species, paralysis.2 The family Argasidae (soft ticks) do not engorge to the same extent as the family Ixodidae (hard ticks) merely taking small, frequent blood meals. In contrast, hard ticks remain attached to host for days and gradually imbibe and metabolise host blood during that time, swelling to their full capacity to retain a reservoir of blood in the last 24 hours or so of attachment. Hard ticks have been the only group encountered at the border so far, and details of their biology and ecology can be readily found.2,5 Sources of ticks Ticks occur in all climatic regions on earth and humans encounter them during their occupations or recreational activities, especially if they brush against vegetation on which questing ticks gather, or if they sleep on open ground4. A thorough search of literature data bases produced published evidence of 390 species of ticks that infest both humans and companion animals around the world (ACG Heath, unpublished). Although 20 of these associations are considered rare, a considerable number of tick species remain about which to be vigilant. The primary hosts of the ticks taken from humans include a large range of vertebrates, although companion animals, especially dogs should be considered as an important means of bringing ticks within the human environment. Close association with livestock and companion animals, as well as yards and kennels can increase the likelihood of ticks being acquired, but only rarely are ticks acquired directly from animals. Ticks usually settle quickly to attach and feed once on a host, and very rarely detach and move during this time so are not usually acquired directly from an infested host. Ticks can also become associated with personal effects, such as clothing and furniture without the owners being aware, and are then introduced into new surroundings after a flight or voyage. Public health risks from exotic tick species Emerging and emergent tick-borne infections are becoming more common among humans as we move into and change landscapes and are brought into contact with arthropod vectors.6 Mosquitoes are viewed as pre-eminent in transmitting viral infections in the South East Asian and Pacific regions7 although ticks are the leading vectors worldwide. In all 19 rickettsioses, 2 ehrlichioses, anaplasmosis, and around 200 tick-borne arboviruses have been associated to date with ticks.6,8 Recent figures9 showed that almost 50% of travellers returning to Europe and North America from the tropics experienced health problems. Tick-borne infections and specifically rickettsial diseases were mentioned as a possible cause of fever and rash but did not feature as highly as other diseases, such as malaria, dengue and enteric fever for example. Arthropod-related skin diseases in travellers returning home ill accounted for 31% of all diagnoses in one worldwide study10 and around 9% of diagnoses in a recent New Zealand study.11 In another12 arthropod bites were among the ten most frequently encountered diagnoses for common skin problems in returning travellers, although tick bites were not considered as common as those associated with sandflies (Phlebotominae, a subfamily of Psychodidae, or moth flies, not Simuliidae as in New Zealand), fleas and mosquitoes. There are numerous tick-borne diseases that New Zealanders could encounter while overseas, but practically, those which occur in Australia, or in tick species most commonly associated with humans entering New Zealand, provide the most risk, with rickettsioses, borreliosis and viruses predominating. There are similar risks for visitors to Europe and Asia13,14 although there are fewer New Zealand travellers to those regions than to Australia.15 Notwithstanding, Rocky Mountain Spotted Fever especially cannot be ignored as a disease that travellers to the USA could encounter and of which they should be aware. The principal tick-borne diseases including rickettsioses, Lyme Disease and those caused by viruses are described and discussed in numerous publications, e.g. 8,16-26. Current travel advice for New Zealand travellers New Zealanders are able to obtain specific recommendations for vaccination and prophylaxis for a variety of diseases that would be encountered overseas.27,28 Until recently advice27 on tick-borne diseases was limited to tick-borne encephalitis (TBE) said to be transmitted by Ixodes ricinus encountered in the new Independent States of the former Soviet Union and Europe and Lyme Disease, transmitted by ticks from deer and wild rodents...[in] Atlantic coast, upper Midwest and western USA as well as parts of Europe and the new Independent States of the former Soviet Union. The rickettsial diseases of scrub typhus and Queensland tick typhus were also mentioned, being more likely to be acquired by travellers who come into contact with the tick vectors when travelling in ...South-east Asia and eastern Australia. Nowhere in this publication was comment made on the possibility that travellers could bring ticks back with them into New Zealand or that ticks in Western Europe also transmit diseases such as TBE and Lyme borreliosis. A book on the history of infectious diseases in the Pacific29 did not mention any risks associated with ticks although mosquito and mite-borne diseases were discussed.Current advice is available for the travelling public on the website (updated 5 March 2010) for the Ministry of Foreign Affairs and Trade.28 There is no specific or general advice concerning ticks or tick-borne disease at this site. These advisories tend to understate the risk to travellers of tick-borne disease, however perusal of any recent text books or reviews6,8,13,16 shows the extent to which humans are potentially at risk to a suite of pathogens, principally those for erhlichiosis, rickettsiosis, babesiosis and numerous viruses. Numbers and species of ticks intercepted at the border Of the 172 reported instances of ticks encountered at the New Zealand border, or beyond to October 2010, humans were the direct route of entry for 66 (38.4%) of these, carrying the ticks on their persons (Table 1). In nearly all cases patients referred themselves to a GP where the tick was removed, although occasionally ticks were removed by the patient and then taken to a GP or clinic or sent direct to one of us. Ticks were also found in personal effects (including a car) on 12 occasions and twice in rooms inhabited by humans. There were also seven instances of dogs that had never left New Zealand becoming infested with ticks which could only have been introduced by human agency, and one instance of personnel in a quarantine facility acquiring ticks brought in with wapiti (Cervus elaphus nelsoni) from Canada. Taken collectively, these records associate humans with 86 tick introductions (50.0 % of all interceptions). In comparison, companion animals (dogs: 64 introductions, cats: four), were a marginally more frequent direct entry route for ticks (i.e. attached to their bodies), and accounted for 41.0% of all introductions30-32 (ACG Heath & S Hardwick unpublished). There were 17 identified species of ticks associated with humans plus 11 infestations where the ticks could be identified only to family or genus (Table 1). The most commonly encountered species on humans in New Zealand is the Australian paralysis tick, Ixodes holocyclus (found 31 times). On two other occasions reported to us, New Zealanders acquired ticks in Australia, removed them there, but exhibited symptoms of tick bite on return home (Table 2). In addition two New Zealand lapidaries acquired ticks (not identified) while in Queensland in 2009, removed them, but suffered raised welts similar to mosquito bites (R Knowles & T Walker, personal communication, 30 October 2010) Country of origin and sources of ticks The most frequent country of origin of ticks found at New Zealands borders is Australia with 92/172 (53.5 % of all interceptions, humans and companion animals etc. combined), followed by 21 records from Oceania/The Pacific (Fiji, American Samoa, Tonga, New Caledonia, Papua New Guinea, Solomon Islands, Vanuatu, Hawaii); 18 from North America (USA, Canada); 16 from Asia/SE Asia (China, Japan, Hong Kong, Singapore, Malaysia, Philippines, Thailand, Taiwan); 7 from Africa (South Africa, Zambia); 5 from Europe (Switzerland, Belgium, Netherlands); 4 from the Indian continent (Pakistan, Nepal); 4 from the United Kingdom; 2 from the Middle East (Israel, Dubai); and 3 records of unknown origin. Records specifically from humans are shown in Table 1. Table 1. Ticks taken directly from humans in New Zealand* Tick species (number of records) Country of origin Disease associations** Ixodes holocyclus (31) Australia Rickettsia australis; paralysis Amblyomma triguttatum triguttatum (5) Australia Coxiella burnetii Amblyomma (?) loculosum (1) Australia None reported Amblyomma spp. (4) Australia Ixodes tasmani (1) Australia R. australis; R. honei Ixodes spp. (1) Australia Haemaphysalis bancrofti (1) Australia None reported Bothriocroton hydrosauri (1) Australia R. honei Ixodidae (3) Australia Rhipicephalus sanguineus (1) PNG R.conorii; R .rickettsii (RMSF);CCHF; paralysis Dermacentor andersoni (1) USA RMSF;&nb

Summary

Abstract

Humans coming into New Zealand occasionally, and unwittingly, bring exotic ticks with them, either attached to their bodies or with luggage. Of the 172 available records for tick interception at New Zealands border, half can be attributed to human agency. Here, together with an outline of tick biology and ecology, we present evidence of at least 17 species of ticks being brought in by humans, with Australia, North America and Asia the most frequent countries of origin. Risks posed by some of the nine species of ticks already in New Zealand are briefly examined. Sites of attachment of ticks and associated symptoms where these have been recorded are presented. Diseases transmitted by ticks and most likely to be encountered by travellers are briefly discussed together with the most practical method of tick removal. A plea is made for practitioners to increase their awareness of the risks to New Zealands biosecurity and public health posed by ticks and to ensure that as many as possible of these unwelcome souvenirs are collected and passed on for identification.

Aim

Method

Results

Conclusion

Author Information

Allen C G Heath, Senior Scientist, AgResearch Ltd, National Centre for Biosecurity and Infectious Disease, Wallaceville, Upper Hutt; Scott Hardwick, Scientist, AgResearch Ltd., Lincoln Research Centre, Lincoln

Acknowledgements

We thank MAF Biosecurity NZ, various colleagues and general practitioners and laboratory personnel who provided ticks and data relating to infestations, especially Ricardo Palma and Rachel Cane and the late Bob Pilgrim. This work was carried out under the Better Border Biosecurity (B3) programme, funded by the Foundation for Research Science and Technology, with additional assistance from MAF Biosecurity New Zealand. We thank Jos 00e9 Derraik for reading and commenting on an earlier version of this paper and thanks to two anonymous referees for their comments. We also thank those who provided information on their tick infestations but wished to retain their anonymity.

Correspondence

Allen Heath, Senior Scientist, AgResearch Ltd, National Centre for Biosecurity and Infectious Disease, PO Box 40063, Wallaceville, Upper Hutt, New Zealand, 5140. Fax: +64 (0)4 5280355

Correspondence Email

allen.heath@agresearch.co.nz

Competing Interests

None

Heath ACG, Palma RL, Cane RP, Hardwick S Checklist of New Zealand ticks (Acari: Ixodidae, Argasidae). Zootaxa 2011 (in press)Sonenshine DE. Biology of ticks, volume 2. Oxford University Press, 1993.MAF Biosecurity New Zealand, Import Health Standards: http://www.biosecurity.govt.nz/enter/personal/pets updated 21 April 2010 [accessed 26 October 2010]Estrada-Pe 00f1a A, Jongjan F. Ticks feeding on humans: a review of records on human-biting Ixodoidea with special reference to pathogen transmission. Exp Appl Acarol 1999;23:685-715.Varma MRG. 1993. Ticks and mites (Acari), In: Medical insects and arachnids, Lane RP, Crosskey RW editors London, Chapman & Hall, 1993:597-658.Telford SR, Goethert HK. Emerging and emergent tick-borne infections, In: Bowman AS, Nuttall PA editors, Ticks, biology, disease and control. Cambridge University Press, 2008:344-76.Barboza P, Tarantola A, Lassel L, Mollet T, Quatresous I, Paquet C. Viroses 00e9mergentes en Asie du Sud-Est et dans le Pacifique. Med Mal Infect.2008;38:513-23.Labuda M, Nuttall PA. Viruses transmitted by ticks In: Bowman AS Nuttall PA, editors, Ticks Biology, Disease and Control, Cambridge, University Press, 2008:253-80.Looke DFM, Robson JMB. Infections in the returned traveler. Med J Aus 2002;177:212-19.Lederman ER, Weld LH, Elyazar IRF, von Sonneburg F, Loutan L, Schwartz E, Keystone JS. Dermatologic conditions of the ill returned traveler: an analysis from the GeoSentinel Surveillance Network. Int J Infect Dis 2008;12:593-602.Shaw MTM, Leggat PA, Weld LH, Williams ML, Cetron MS. Illness in returned travellers presenting at GeoSentinel sites in New Zealand. Aust NZ J Public Health 2003;27:82-86.OBrien BM. A practical approach to common skin problems in returning travellers. Travel Med Infect Dis 2009;7:125-46.Mackenzie JS, Williams DT. The zoonotic flaviviruses of southern, south-eastern and eastern Asia, and Australasia: the potential for emergent viruses. Zoonoses Public Health 2009;56:338-56.Dobler G. Zoonotic tick-borne flaviviruses. Vet Microbiol 2010;140:221-28.Statistics New Zealandhttp://www.stats.govt.nz/browse_for_stats/population/Migration/IntTravelAndMigration_HOTPJune2010/Commentary.aspxJune 2010 [accessed 26 October 2010]Parola P, Paddock CD, Raoult D. Tick-borne rickettsioses around the world: emerging diseases challenging old concepts. Clin Microbiol Rev 2005;18:719-56.Paddock CD. The science and fiction of emerging rickettsioses. Ann N Y Acad Sci 2009;1166:133-43.Graves S, Stenos J. Rickettsioses in Australia. Ann N Y Acad Sci 2009;1166:151-55.Hilbink F, Penrose M, Kovacova E, Kazar J. Q fever is absent from New Zealand. Int J Epidemiol 1993;22:945-49.Greenslade E, Beasley R, Jennings L, Woodward A, Weinstein P. Has Coxiella burnetii (Q fever) been introduced into New Zealand? Emerg Infect Dis 2003;9:138-40.Arricau-Bouvery N, Rodolakis A. Is Q fever an emerging or re-emerging zoonosis? Vet Res 2005;36:327-49.Heath ACG. Vector competence of Haemaphysalis longicornis with particular reference to blood parasites. Surveillance 2002;29 (4):12-14.Piesman J, Gern L. Lyme borreliosis in Europe and North America, Parasitology 2004;129:S191-S220.Olsen B, Duffy DC, Jaenson TGT, Oylfe A, Bonnedahl J, Bergstrom S. Transhemispheric exchange of Lyme disease spriochetes by seabirds. J Clin Microbiol 1995;3:3270-74.Russell RC. Vectors vs. humans in Australia - who is on top down under? An update on vector-borne disease and research on vectors in Australia. J Vector Ecol 1998;23:1-46.Port Macquarie News: (http://www.portnews.com.au/news/local/news/general/diagnosis-positive-tick-disease-is-here/1944198.aspx 17 September 2010 [accessed 26 October 2010]Ellis-Pegler R, Ingram J. Health advice for overseas travellers. Wellington: Ministry of Health, 1996.New Zealand Ministry of Foreign Affair and Trade http://www.safetravel.govt.nz/ updated 3 March 2010 [accessed 26 October 2010]Miles J. Infectious diseases: colonising the Pacific? Dunedin, University of Otago Press, 1997.Fairley R., Heath ACG. Exotic ticks intercepted in New Zealand since 1980. Surveillance 1997;24(1):21-22.Heath ACG. Exotic tick interceptions 1980-2000. Surveillance 2001:28(4):13-15.Loth L. Review of exotic tick interceptions in New Zealand since 1980. Surveillance 2005;32(3):7-9.New Zealand Ministry of Tourism statistics; http://www.tourismresearch.govt.nz/Morrissey T. Intelligence at the border. Biosecurity 2010;100:3Roberts FHS. Australian ticks. Melbourne, CSIRO, 1970.Waudby HP, Petit S, Weber D. Human perception and awareness of ticks in a South Australian rural community and implications for management of Amblyomma triguttatum triguttatum. Exp Appl Acarol. 2008;45:71-84.Sexton DJ, Dwyer B, Kemp R, Graves S. Spotted fever group rickettsial infections in Australia. Rev Infect Dis. 1991;13:876-86.Pearce RL, Grove DI. Tick infestation in soldiers who were bivouacked in the Perth region. Med J Aust. 1987 146:238-40Miller MK. Massive tick (Ixodes holocyclus) infestation with delayed facial-nerve palsy. Med J Aust. 2002;176:264-5.Sutherland SK. Ticks, In: Sutherland SK, editor, Australian animal toxins: the creatures, their toxins and care of the poisoned patient. Melbourne, Oxford University Press, 1983;299-315.Centers for Disease Control and Prevention, Department of Health and Human Services, USA;http://www.cdc.gov/ticks/diseases/ Updated September 2010 [accessed 26 October 2010]Mans BJ, Gothe R, Neitz WH. Tick toxins: perspectives on paralysis and other forms of toxicoses caused by ticks. In: Bowman AS, Nuttall PA, editors, Ticks, biology, disease and control, Cambridge University Press, 2008:108-26.Gratton-Smith PJ, Morris JG, Johnston HM, Yiannikas C, Malik R, Russell R, Ouvrier RA. Clinical and neurophysiological features of tick paralysis, Brain 1997;120:1975-87.Brown FT, Hamilton DL. Tick bite anaphylaxis in Australia. J Accid Emerg Med 1997;15:111-13.Rowe RS. 1980. Cattle tick infestation. N Z Med J 91, 472-473.Heath ACG. 1986. Interception of the brown dog tick, Rhipicephalus sanguineus infesting man. N Z Vet J 34,76-77.Humphery-Smith I, Cybinski DH. Health risks from tick-transmitted arboviruses on Australias Great Barrier Reef. Med J Aust. 1987;146:606-7.Humphery-Smith I, Cybinski DH, Moorhouse DE, Dale D. Arboviruses and zoonotic infections on the Great Barrier Reef and in the Coral Sea. Arbovirus Research in Australia, Proceedings 4th Symposium, 1986:209-17.Oxer DT, Ricardo CL. 1942. Notes on the biology, toxicity and breeding of Ixodes holocyclus (Neumann). Aust Vet J 18, 194-199.Sutherst RW, Moorhouse DE. 1971. Ixodes holocyclus larvae and scrub-itch- in south-east Queensland. Southeast Asian J Trop Med Public Health 2, 82-83.Moorhouse DE. Ticks and their medical importance, In: Pearn J, editor, Animal Toxins and Man, Brisbane, Queensland Health Department, 1981:63-9.Gauci M, Loh RKS, Stone BF, Thong YH. Allergic reaction to the Australian paralysis tick, Ixodes holocyclus: diagnostic evaluation by skin test and radioimmunoassay. Clin Exp Allergy 1989;19:279-283.Unsworth N, Graves S, Nguyen C, Kemp G, Graham J, Stenos J. 2008. Markers of exposure to spotted fever rickettsiae in patients with chronic illness, including fatigue, in two Australian populations. Queensland J Med, 101, 269-274.Zenner L, Drevon-Gaillot E, Callait-Cardinal MP. Evaluation of four manual tick-removal devices for dogs and cats. Vet Rec. 2006;159:526-29.Theis JH. Mechanical removal of Rhipicephalus sanguineus from the dog. J Am Vet Med Assoc. 1968;153:433-37.Austin FJ. Ticks as arbovirus vectors in New Zealand. N Z Entomol. 1984;8:105-6.Humphery-Smith I, Thong YH, Moorhouse D, Creevey C. Reactions to argasid tick bites by island residents on the Great Barrier Reef. Med J Aust. 1991;155:181-6.Mackereth G, Cane R, Snell-Wakefield A, et al. Vectors and vector-borne diseases: Ecological research and surveillance development in New Zealand, risk assessment. Biosecurity New Zealand, Ministry of Agriculture and Forestry, unpublished report, June 2007:1-64.Myers JG. The cattle-tick (Haemaphysalis bispinosa). Investigations during 1923-24. New Zealand Department of Agriculture, bulletin 1924;116:1-105.Heath ACG. The temperature and humidity preferences of Haemaphysalis longicornis, Ixodes holocyclus and Rhipicephalus sanguineus (Ixodidae): studies on eggs. Int J Parasitol 1979;9:33-9.

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Check out the new and updated website of the National Alliance of Safe Pest Control: http://www.pests.org The world tick fauna comprises about 900 species of which New Zealand has 11 confirmed.1 Four of these are endemic (kiwi tick, Ixodes anatis; tuatara tick, Amblyomma (formerly Aponomma)sphenodonti and the cormorant tick, I. jacksoni), as well as a new species of Carios from a native bat, and the others are either exotic (Carios (formerly Ornithodoros) capensis, Haemaphysalis longicornis, Ixodes amersoni ) or shared with Australia (Ixodes eudyptidis), or distributed throughout the sub-Antarctic faunal region (I. kerguelenensis, I. auritulus zealandicus, and I. uriae). OnlyH. longicornis has been recorded from humans in New Zealand, with C. capensis capable but not reported doing so in this country. Figure 1. Engorged female New Zealand cattle tick, Haemaphysalis longicornis (left); and (right) male (small tick) and engorged female paralysis ticks, Ixodes holocyclus (photos courtesy of Wikipedia under the Creative Commons Attribution-Share Alike 3.0 Unported license) Ticks are of considerable economic importance as far as livestock are concerned2 and stringent measures are employed to keep these exotic parasites out of New Zealand. Companion and other live animals imported into New Zealand are subject to import health standards that comprise pre-export treatment with an acaricide, as well as veterinary inspection and clearance. Companion animal imports from countries where rabies is endemic are also subject to quarantine.3 Humans are not subject to such measures but worldwide, are an important pathway for exotic ticks.4 By travelling extensively, New Zealanders increase their risk of being infested by ticks and catching tick-borne disease. First we outline the biology, ecology and diseases associated with ticks and then we review details of all instances that we could find of exotic ticks found on travellers that had entered New Zealand, or which were associated with their belongings or activities, both to draw the attention of the medical profession to the magnitude of this problem, and to raise awareness of the risks posed to public health. The vector potential of ticks that occur in New Zealand is also discussed. Tick biology Ticks are arthropods that require blood to survive and reproduce. This characteristic and their often remarkable longevity make them ideal candidates for the transmission of many types of disease organisms. In addition, ticks can also cause a variety of medical conditions ranging from localised irritation to anaemia and, with some species, paralysis.2 The family Argasidae (soft ticks) do not engorge to the same extent as the family Ixodidae (hard ticks) merely taking small, frequent blood meals. In contrast, hard ticks remain attached to host for days and gradually imbibe and metabolise host blood during that time, swelling to their full capacity to retain a reservoir of blood in the last 24 hours or so of attachment. Hard ticks have been the only group encountered at the border so far, and details of their biology and ecology can be readily found.2,5 Sources of ticks Ticks occur in all climatic regions on earth and humans encounter them during their occupations or recreational activities, especially if they brush against vegetation on which questing ticks gather, or if they sleep on open ground4. A thorough search of literature data bases produced published evidence of 390 species of ticks that infest both humans and companion animals around the world (ACG Heath, unpublished). Although 20 of these associations are considered rare, a considerable number of tick species remain about which to be vigilant. The primary hosts of the ticks taken from humans include a large range of vertebrates, although companion animals, especially dogs should be considered as an important means of bringing ticks within the human environment. Close association with livestock and companion animals, as well as yards and kennels can increase the likelihood of ticks being acquired, but only rarely are ticks acquired directly from animals. Ticks usually settle quickly to attach and feed once on a host, and very rarely detach and move during this time so are not usually acquired directly from an infested host. Ticks can also become associated with personal effects, such as clothing and furniture without the owners being aware, and are then introduced into new surroundings after a flight or voyage. Public health risks from exotic tick species Emerging and emergent tick-borne infections are becoming more common among humans as we move into and change landscapes and are brought into contact with arthropod vectors.6 Mosquitoes are viewed as pre-eminent in transmitting viral infections in the South East Asian and Pacific regions7 although ticks are the leading vectors worldwide. In all 19 rickettsioses, 2 ehrlichioses, anaplasmosis, and around 200 tick-borne arboviruses have been associated to date with ticks.6,8 Recent figures9 showed that almost 50% of travellers returning to Europe and North America from the tropics experienced health problems. Tick-borne infections and specifically rickettsial diseases were mentioned as a possible cause of fever and rash but did not feature as highly as other diseases, such as malaria, dengue and enteric fever for example. Arthropod-related skin diseases in travellers returning home ill accounted for 31% of all diagnoses in one worldwide study10 and around 9% of diagnoses in a recent New Zealand study.11 In another12 arthropod bites were among the ten most frequently encountered diagnoses for common skin problems in returning travellers, although tick bites were not considered as common as those associated with sandflies (Phlebotominae, a subfamily of Psychodidae, or moth flies, not Simuliidae as in New Zealand), fleas and mosquitoes. There are numerous tick-borne diseases that New Zealanders could encounter while overseas, but practically, those which occur in Australia, or in tick species most commonly associated with humans entering New Zealand, provide the most risk, with rickettsioses, borreliosis and viruses predominating. There are similar risks for visitors to Europe and Asia13,14 although there are fewer New Zealand travellers to those regions than to Australia.15 Notwithstanding, Rocky Mountain Spotted Fever especially cannot be ignored as a disease that travellers to the USA could encounter and of which they should be aware. The principal tick-borne diseases including rickettsioses, Lyme Disease and those caused by viruses are described and discussed in numerous publications, e.g. 8,16-26. Current travel advice for New Zealand travellers New Zealanders are able to obtain specific recommendations for vaccination and prophylaxis for a variety of diseases that would be encountered overseas.27,28 Until recently advice27 on tick-borne diseases was limited to tick-borne encephalitis (TBE) said to be transmitted by Ixodes ricinus encountered in the new Independent States of the former Soviet Union and Europe and Lyme Disease, transmitted by ticks from deer and wild rodents...[in] Atlantic coast, upper Midwest and western USA as well as parts of Europe and the new Independent States of the former Soviet Union. The rickettsial diseases of scrub typhus and Queensland tick typhus were also mentioned, being more likely to be acquired by travellers who come into contact with the tick vectors when travelling in ...South-east Asia and eastern Australia. Nowhere in this publication was comment made on the possibility that travellers could bring ticks back with them into New Zealand or that ticks in Western Europe also transmit diseases such as TBE and Lyme borreliosis. A book on the history of infectious diseases in the Pacific29 did not mention any risks associated with ticks although mosquito and mite-borne diseases were discussed.Current advice is available for the travelling public on the website (updated 5 March 2010) for the Ministry of Foreign Affairs and Trade.28 There is no specific or general advice concerning ticks or tick-borne disease at this site. These advisories tend to understate the risk to travellers of tick-borne disease, however perusal of any recent text books or reviews6,8,13,16 shows the extent to which humans are potentially at risk to a suite of pathogens, principally those for erhlichiosis, rickettsiosis, babesiosis and numerous viruses. Numbers and species of ticks intercepted at the border Of the 172 reported instances of ticks encountered at the New Zealand border, or beyond to October 2010, humans were the direct route of entry for 66 (38.4%) of these, carrying the ticks on their persons (Table 1). In nearly all cases patients referred themselves to a GP where the tick was removed, although occasionally ticks were removed by the patient and then taken to a GP or clinic or sent direct to one of us. Ticks were also found in personal effects (including a car) on 12 occasions and twice in rooms inhabited by humans. There were also seven instances of dogs that had never left New Zealand becoming infested with ticks which could only have been introduced by human agency, and one instance of personnel in a quarantine facility acquiring ticks brought in with wapiti (Cervus elaphus nelsoni) from Canada. Taken collectively, these records associate humans with 86 tick introductions (50.0 % of all interceptions). In comparison, companion animals (dogs: 64 introductions, cats: four), were a marginally more frequent direct entry route for ticks (i.e. attached to their bodies), and accounted for 41.0% of all introductions30-32 (ACG Heath & S Hardwick unpublished). There were 17 identified species of ticks associated with humans plus 11 infestations where the ticks could be identified only to family or genus (Table 1). The most commonly encountered species on humans in New Zealand is the Australian paralysis tick, Ixodes holocyclus (found 31 times). On two other occasions reported to us, New Zealanders acquired ticks in Australia, removed them there, but exhibited symptoms of tick bite on return home (Table 2). In addition two New Zealand lapidaries acquired ticks (not identified) while in Queensland in 2009, removed them, but suffered raised welts similar to mosquito bites (R Knowles & T Walker, personal communication, 30 October 2010) Country of origin and sources of ticks The most frequent country of origin of ticks found at New Zealands borders is Australia with 92/172 (53.5 % of all interceptions, humans and companion animals etc. combined), followed by 21 records from Oceania/The Pacific (Fiji, American Samoa, Tonga, New Caledonia, Papua New Guinea, Solomon Islands, Vanuatu, Hawaii); 18 from North America (USA, Canada); 16 from Asia/SE Asia (China, Japan, Hong Kong, Singapore, Malaysia, Philippines, Thailand, Taiwan); 7 from Africa (South Africa, Zambia); 5 from Europe (Switzerland, Belgium, Netherlands); 4 from the Indian continent (Pakistan, Nepal); 4 from the United Kingdom; 2 from the Middle East (Israel, Dubai); and 3 records of unknown origin. Records specifically from humans are shown in Table 1. Table 1. Ticks taken directly from humans in New Zealand* Tick species (number of records) Country of origin Disease associations** Ixodes holocyclus (31) Australia Rickettsia australis; paralysis Amblyomma triguttatum triguttatum (5) Australia Coxiella burnetii Amblyomma (?) loculosum (1) Australia None reported Amblyomma spp. (4) Australia Ixodes tasmani (1) Australia R. australis; R. honei Ixodes spp. (1) Australia Haemaphysalis bancrofti (1) Australia None reported Bothriocroton hydrosauri (1) Australia R. honei Ixodidae (3) Australia Rhipicephalus sanguineus (1) PNG R.conorii; R .rickettsii (RMSF);CCHF; paralysis Dermacentor andersoni (1) USA RMSF;&nb

Summary

Abstract

Humans coming into New Zealand occasionally, and unwittingly, bring exotic ticks with them, either attached to their bodies or with luggage. Of the 172 available records for tick interception at New Zealands border, half can be attributed to human agency. Here, together with an outline of tick biology and ecology, we present evidence of at least 17 species of ticks being brought in by humans, with Australia, North America and Asia the most frequent countries of origin. Risks posed by some of the nine species of ticks already in New Zealand are briefly examined. Sites of attachment of ticks and associated symptoms where these have been recorded are presented. Diseases transmitted by ticks and most likely to be encountered by travellers are briefly discussed together with the most practical method of tick removal. A plea is made for practitioners to increase their awareness of the risks to New Zealands biosecurity and public health posed by ticks and to ensure that as many as possible of these unwelcome souvenirs are collected and passed on for identification.

Aim

Method

Results

Conclusion

Author Information

Allen C G Heath, Senior Scientist, AgResearch Ltd, National Centre for Biosecurity and Infectious Disease, Wallaceville, Upper Hutt; Scott Hardwick, Scientist, AgResearch Ltd., Lincoln Research Centre, Lincoln

Acknowledgements

We thank MAF Biosecurity NZ, various colleagues and general practitioners and laboratory personnel who provided ticks and data relating to infestations, especially Ricardo Palma and Rachel Cane and the late Bob Pilgrim. This work was carried out under the Better Border Biosecurity (B3) programme, funded by the Foundation for Research Science and Technology, with additional assistance from MAF Biosecurity New Zealand. We thank Jos 00e9 Derraik for reading and commenting on an earlier version of this paper and thanks to two anonymous referees for their comments. We also thank those who provided information on their tick infestations but wished to retain their anonymity.

Correspondence

Allen Heath, Senior Scientist, AgResearch Ltd, National Centre for Biosecurity and Infectious Disease, PO Box 40063, Wallaceville, Upper Hutt, New Zealand, 5140. Fax: +64 (0)4 5280355

Correspondence Email

allen.heath@agresearch.co.nz

Competing Interests

None

Heath ACG, Palma RL, Cane RP, Hardwick S Checklist of New Zealand ticks (Acari: Ixodidae, Argasidae). Zootaxa 2011 (in press)Sonenshine DE. Biology of ticks, volume 2. Oxford University Press, 1993.MAF Biosecurity New Zealand, Import Health Standards: http://www.biosecurity.govt.nz/enter/personal/pets updated 21 April 2010 [accessed 26 October 2010]Estrada-Pe 00f1a A, Jongjan F. Ticks feeding on humans: a review of records on human-biting Ixodoidea with special reference to pathogen transmission. Exp Appl Acarol 1999;23:685-715.Varma MRG. 1993. Ticks and mites (Acari), In: Medical insects and arachnids, Lane RP, Crosskey RW editors London, Chapman & Hall, 1993:597-658.Telford SR, Goethert HK. Emerging and emergent tick-borne infections, In: Bowman AS, Nuttall PA editors, Ticks, biology, disease and control. Cambridge University Press, 2008:344-76.Barboza P, Tarantola A, Lassel L, Mollet T, Quatresous I, Paquet C. Viroses 00e9mergentes en Asie du Sud-Est et dans le Pacifique. Med Mal Infect.2008;38:513-23.Labuda M, Nuttall PA. Viruses transmitted by ticks In: Bowman AS Nuttall PA, editors, Ticks Biology, Disease and Control, Cambridge, University Press, 2008:253-80.Looke DFM, Robson JMB. Infections in the returned traveler. Med J Aus 2002;177:212-19.Lederman ER, Weld LH, Elyazar IRF, von Sonneburg F, Loutan L, Schwartz E, Keystone JS. Dermatologic conditions of the ill returned traveler: an analysis from the GeoSentinel Surveillance Network. Int J Infect Dis 2008;12:593-602.Shaw MTM, Leggat PA, Weld LH, Williams ML, Cetron MS. Illness in returned travellers presenting at GeoSentinel sites in New Zealand. Aust NZ J Public Health 2003;27:82-86.OBrien BM. A practical approach to common skin problems in returning travellers. Travel Med Infect Dis 2009;7:125-46.Mackenzie JS, Williams DT. The zoonotic flaviviruses of southern, south-eastern and eastern Asia, and Australasia: the potential for emergent viruses. Zoonoses Public Health 2009;56:338-56.Dobler G. Zoonotic tick-borne flaviviruses. Vet Microbiol 2010;140:221-28.Statistics New Zealandhttp://www.stats.govt.nz/browse_for_stats/population/Migration/IntTravelAndMigration_HOTPJune2010/Commentary.aspxJune 2010 [accessed 26 October 2010]Parola P, Paddock CD, Raoult D. Tick-borne rickettsioses around the world: emerging diseases challenging old concepts. Clin Microbiol Rev 2005;18:719-56.Paddock CD. The science and fiction of emerging rickettsioses. Ann N Y Acad Sci 2009;1166:133-43.Graves S, Stenos J. Rickettsioses in Australia. Ann N Y Acad Sci 2009;1166:151-55.Hilbink F, Penrose M, Kovacova E, Kazar J. Q fever is absent from New Zealand. Int J Epidemiol 1993;22:945-49.Greenslade E, Beasley R, Jennings L, Woodward A, Weinstein P. Has Coxiella burnetii (Q fever) been introduced into New Zealand? Emerg Infect Dis 2003;9:138-40.Arricau-Bouvery N, Rodolakis A. Is Q fever an emerging or re-emerging zoonosis? Vet Res 2005;36:327-49.Heath ACG. Vector competence of Haemaphysalis longicornis with particular reference to blood parasites. Surveillance 2002;29 (4):12-14.Piesman J, Gern L. Lyme borreliosis in Europe and North America, Parasitology 2004;129:S191-S220.Olsen B, Duffy DC, Jaenson TGT, Oylfe A, Bonnedahl J, Bergstrom S. Transhemispheric exchange of Lyme disease spriochetes by seabirds. J Clin Microbiol 1995;3:3270-74.Russell RC. Vectors vs. humans in Australia - who is on top down under? An update on vector-borne disease and research on vectors in Australia. J Vector Ecol 1998;23:1-46.Port Macquarie News: (http://www.portnews.com.au/news/local/news/general/diagnosis-positive-tick-disease-is-here/1944198.aspx 17 September 2010 [accessed 26 October 2010]Ellis-Pegler R, Ingram J. Health advice for overseas travellers. Wellington: Ministry of Health, 1996.New Zealand Ministry of Foreign Affair and Trade http://www.safetravel.govt.nz/ updated 3 March 2010 [accessed 26 October 2010]Miles J. Infectious diseases: colonising the Pacific? Dunedin, University of Otago Press, 1997.Fairley R., Heath ACG. Exotic ticks intercepted in New Zealand since 1980. Surveillance 1997;24(1):21-22.Heath ACG. Exotic tick interceptions 1980-2000. Surveillance 2001:28(4):13-15.Loth L. Review of exotic tick interceptions in New Zealand since 1980. Surveillance 2005;32(3):7-9.New Zealand Ministry of Tourism statistics; http://www.tourismresearch.govt.nz/Morrissey T. Intelligence at the border. Biosecurity 2010;100:3Roberts FHS. Australian ticks. Melbourne, CSIRO, 1970.Waudby HP, Petit S, Weber D. Human perception and awareness of ticks in a South Australian rural community and implications for management of Amblyomma triguttatum triguttatum. Exp Appl Acarol. 2008;45:71-84.Sexton DJ, Dwyer B, Kemp R, Graves S. Spotted fever group rickettsial infections in Australia. Rev Infect Dis. 1991;13:876-86.Pearce RL, Grove DI. Tick infestation in soldiers who were bivouacked in the Perth region. Med J Aust. 1987 146:238-40Miller MK. Massive tick (Ixodes holocyclus) infestation with delayed facial-nerve palsy. Med J Aust. 2002;176:264-5.Sutherland SK. Ticks, In: Sutherland SK, editor, Australian animal toxins: the creatures, their toxins and care of the poisoned patient. Melbourne, Oxford University Press, 1983;299-315.Centers for Disease Control and Prevention, Department of Health and Human Services, USA;http://www.cdc.gov/ticks/diseases/ Updated September 2010 [accessed 26 October 2010]Mans BJ, Gothe R, Neitz WH. Tick toxins: perspectives on paralysis and other forms of toxicoses caused by ticks. In: Bowman AS, Nuttall PA, editors, Ticks, biology, disease and control, Cambridge University Press, 2008:108-26.Gratton-Smith PJ, Morris JG, Johnston HM, Yiannikas C, Malik R, Russell R, Ouvrier RA. Clinical and neurophysiological features of tick paralysis, Brain 1997;120:1975-87.Brown FT, Hamilton DL. Tick bite anaphylaxis in Australia. J Accid Emerg Med 1997;15:111-13.Rowe RS. 1980. Cattle tick infestation. N Z Med J 91, 472-473.Heath ACG. 1986. Interception of the brown dog tick, Rhipicephalus sanguineus infesting man. N Z Vet J 34,76-77.Humphery-Smith I, Cybinski DH. Health risks from tick-transmitted arboviruses on Australias Great Barrier Reef. Med J Aust. 1987;146:606-7.Humphery-Smith I, Cybinski DH, Moorhouse DE, Dale D. Arboviruses and zoonotic infections on the Great Barrier Reef and in the Coral Sea. Arbovirus Research in Australia, Proceedings 4th Symposium, 1986:209-17.Oxer DT, Ricardo CL. 1942. Notes on the biology, toxicity and breeding of Ixodes holocyclus (Neumann). Aust Vet J 18, 194-199.Sutherst RW, Moorhouse DE. 1971. Ixodes holocyclus larvae and scrub-itch- in south-east Queensland. Southeast Asian J Trop Med Public Health 2, 82-83.Moorhouse DE. Ticks and their medical importance, In: Pearn J, editor, Animal Toxins and Man, Brisbane, Queensland Health Department, 1981:63-9.Gauci M, Loh RKS, Stone BF, Thong YH. Allergic reaction to the Australian paralysis tick, Ixodes holocyclus: diagnostic evaluation by skin test and radioimmunoassay. Clin Exp Allergy 1989;19:279-283.Unsworth N, Graves S, Nguyen C, Kemp G, Graham J, Stenos J. 2008. Markers of exposure to spotted fever rickettsiae in patients with chronic illness, including fatigue, in two Australian populations. Queensland J Med, 101, 269-274.Zenner L, Drevon-Gaillot E, Callait-Cardinal MP. Evaluation of four manual tick-removal devices for dogs and cats. Vet Rec. 2006;159:526-29.Theis JH. Mechanical removal of Rhipicephalus sanguineus from the dog. J Am Vet Med Assoc. 1968;153:433-37.Austin FJ. Ticks as arbovirus vectors in New Zealand. N Z Entomol. 1984;8:105-6.Humphery-Smith I, Thong YH, Moorhouse D, Creevey C. Reactions to argasid tick bites by island residents on the Great Barrier Reef. Med J Aust. 1991;155:181-6.Mackereth G, Cane R, Snell-Wakefield A, et al. Vectors and vector-borne diseases: Ecological research and surveillance development in New Zealand, risk assessment. Biosecurity New Zealand, Ministry of Agriculture and Forestry, unpublished report, June 2007:1-64.Myers JG. The cattle-tick (Haemaphysalis bispinosa). Investigations during 1923-24. New Zealand Department of Agriculture, bulletin 1924;116:1-105.Heath ACG. The temperature and humidity preferences of Haemaphysalis longicornis, Ixodes holocyclus and Rhipicephalus sanguineus (Ixodidae): studies on eggs. Int J Parasitol 1979;9:33-9.

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Check out the new and updated website of the National Alliance of Safe Pest Control: http://www.pests.org The world tick fauna comprises about 900 species of which New Zealand has 11 confirmed.1 Four of these are endemic (kiwi tick, Ixodes anatis; tuatara tick, Amblyomma (formerly Aponomma)sphenodonti and the cormorant tick, I. jacksoni), as well as a new species of Carios from a native bat, and the others are either exotic (Carios (formerly Ornithodoros) capensis, Haemaphysalis longicornis, Ixodes amersoni ) or shared with Australia (Ixodes eudyptidis), or distributed throughout the sub-Antarctic faunal region (I. kerguelenensis, I. auritulus zealandicus, and I. uriae). OnlyH. longicornis has been recorded from humans in New Zealand, with C. capensis capable but not reported doing so in this country. Figure 1. Engorged female New Zealand cattle tick, Haemaphysalis longicornis (left); and (right) male (small tick) and engorged female paralysis ticks, Ixodes holocyclus (photos courtesy of Wikipedia under the Creative Commons Attribution-Share Alike 3.0 Unported license) Ticks are of considerable economic importance as far as livestock are concerned2 and stringent measures are employed to keep these exotic parasites out of New Zealand. Companion and other live animals imported into New Zealand are subject to import health standards that comprise pre-export treatment with an acaricide, as well as veterinary inspection and clearance. Companion animal imports from countries where rabies is endemic are also subject to quarantine.3 Humans are not subject to such measures but worldwide, are an important pathway for exotic ticks.4 By travelling extensively, New Zealanders increase their risk of being infested by ticks and catching tick-borne disease. First we outline the biology, ecology and diseases associated with ticks and then we review details of all instances that we could find of exotic ticks found on travellers that had entered New Zealand, or which were associated with their belongings or activities, both to draw the attention of the medical profession to the magnitude of this problem, and to raise awareness of the risks posed to public health. The vector potential of ticks that occur in New Zealand is also discussed. Tick biology Ticks are arthropods that require blood to survive and reproduce. This characteristic and their often remarkable longevity make them ideal candidates for the transmission of many types of disease organisms. In addition, ticks can also cause a variety of medical conditions ranging from localised irritation to anaemia and, with some species, paralysis.2 The family Argasidae (soft ticks) do not engorge to the same extent as the family Ixodidae (hard ticks) merely taking small, frequent blood meals. In contrast, hard ticks remain attached to host for days and gradually imbibe and metabolise host blood during that time, swelling to their full capacity to retain a reservoir of blood in the last 24 hours or so of attachment. Hard ticks have been the only group encountered at the border so far, and details of their biology and ecology can be readily found.2,5 Sources of ticks Ticks occur in all climatic regions on earth and humans encounter them during their occupations or recreational activities, especially if they brush against vegetation on which questing ticks gather, or if they sleep on open ground4. A thorough search of literature data bases produced published evidence of 390 species of ticks that infest both humans and companion animals around the world (ACG Heath, unpublished). Although 20 of these associations are considered rare, a considerable number of tick species remain about which to be vigilant. The primary hosts of the ticks taken from humans include a large range of vertebrates, although companion animals, especially dogs should be considered as an important means of bringing ticks within the human environment. Close association with livestock and companion animals, as well as yards and kennels can increase the likelihood of ticks being acquired, but only rarely are ticks acquired directly from animals. Ticks usually settle quickly to attach and feed once on a host, and very rarely detach and move during this time so are not usually acquired directly from an infested host. Ticks can also become associated with personal effects, such as clothing and furniture without the owners being aware, and are then introduced into new surroundings after a flight or voyage. Public health risks from exotic tick species Emerging and emergent tick-borne infections are becoming more common among humans as we move into and change landscapes and are brought into contact with arthropod vectors.6 Mosquitoes are viewed as pre-eminent in transmitting viral infections in the South East Asian and Pacific regions7 although ticks are the leading vectors worldwide. In all 19 rickettsioses, 2 ehrlichioses, anaplasmosis, and around 200 tick-borne arboviruses have been associated to date with ticks.6,8 Recent figures9 showed that almost 50% of travellers returning to Europe and North America from the tropics experienced health problems. Tick-borne infections and specifically rickettsial diseases were mentioned as a possible cause of fever and rash but did not feature as highly as other diseases, such as malaria, dengue and enteric fever for example. Arthropod-related skin diseases in travellers returning home ill accounted for 31% of all diagnoses in one worldwide study10 and around 9% of diagnoses in a recent New Zealand study.11 In another12 arthropod bites were among the ten most frequently encountered diagnoses for common skin problems in returning travellers, although tick bites were not considered as common as those associated with sandflies (Phlebotominae, a subfamily of Psychodidae, or moth flies, not Simuliidae as in New Zealand), fleas and mosquitoes. There are numerous tick-borne diseases that New Zealanders could encounter while overseas, but practically, those which occur in Australia, or in tick species most commonly associated with humans entering New Zealand, provide the most risk, with rickettsioses, borreliosis and viruses predominating. There are similar risks for visitors to Europe and Asia13,14 although there are fewer New Zealand travellers to those regions than to Australia.15 Notwithstanding, Rocky Mountain Spotted Fever especially cannot be ignored as a disease that travellers to the USA could encounter and of which they should be aware. The principal tick-borne diseases including rickettsioses, Lyme Disease and those caused by viruses are described and discussed in numerous publications, e.g. 8,16-26. Current travel advice for New Zealand travellers New Zealanders are able to obtain specific recommendations for vaccination and prophylaxis for a variety of diseases that would be encountered overseas.27,28 Until recently advice27 on tick-borne diseases was limited to tick-borne encephalitis (TBE) said to be transmitted by Ixodes ricinus encountered in the new Independent States of the former Soviet Union and Europe and Lyme Disease, transmitted by ticks from deer and wild rodents...[in] Atlantic coast, upper Midwest and western USA as well as parts of Europe and the new Independent States of the former Soviet Union. The rickettsial diseases of scrub typhus and Queensland tick typhus were also mentioned, being more likely to be acquired by travellers who come into contact with the tick vectors when travelling in ...South-east Asia and eastern Australia. Nowhere in this publication was comment made on the possibility that travellers could bring ticks back with them into New Zealand or that ticks in Western Europe also transmit diseases such as TBE and Lyme borreliosis. A book on the history of infectious diseases in the Pacific29 did not mention any risks associated with ticks although mosquito and mite-borne diseases were discussed.Current advice is available for the travelling public on the website (updated 5 March 2010) for the Ministry of Foreign Affairs and Trade.28 There is no specific or general advice concerning ticks or tick-borne disease at this site. These advisories tend to understate the risk to travellers of tick-borne disease, however perusal of any recent text books or reviews6,8,13,16 shows the extent to which humans are potentially at risk to a suite of pathogens, principally those for erhlichiosis, rickettsiosis, babesiosis and numerous viruses. Numbers and species of ticks intercepted at the border Of the 172 reported instances of ticks encountered at the New Zealand border, or beyond to October 2010, humans were the direct route of entry for 66 (38.4%) of these, carrying the ticks on their persons (Table 1). In nearly all cases patients referred themselves to a GP where the tick was removed, although occasionally ticks were removed by the patient and then taken to a GP or clinic or sent direct to one of us. Ticks were also found in personal effects (including a car) on 12 occasions and twice in rooms inhabited by humans. There were also seven instances of dogs that had never left New Zealand becoming infested with ticks which could only have been introduced by human agency, and one instance of personnel in a quarantine facility acquiring ticks brought in with wapiti (Cervus elaphus nelsoni) from Canada. Taken collectively, these records associate humans with 86 tick introductions (50.0 % of all interceptions). In comparison, companion animals (dogs: 64 introductions, cats: four), were a marginally more frequent direct entry route for ticks (i.e. attached to their bodies), and accounted for 41.0% of all introductions30-32 (ACG Heath & S Hardwick unpublished). There were 17 identified species of ticks associated with humans plus 11 infestations where the ticks could be identified only to family or genus (Table 1). The most commonly encountered species on humans in New Zealand is the Australian paralysis tick, Ixodes holocyclus (found 31 times). On two other occasions reported to us, New Zealanders acquired ticks in Australia, removed them there, but exhibited symptoms of tick bite on return home (Table 2). In addition two New Zealand lapidaries acquired ticks (not identified) while in Queensland in 2009, removed them, but suffered raised welts similar to mosquito bites (R Knowles & T Walker, personal communication, 30 October 2010) Country of origin and sources of ticks The most frequent country of origin of ticks found at New Zealands borders is Australia with 92/172 (53.5 % of all interceptions, humans and companion animals etc. combined), followed by 21 records from Oceania/The Pacific (Fiji, American Samoa, Tonga, New Caledonia, Papua New Guinea, Solomon Islands, Vanuatu, Hawaii); 18 from North America (USA, Canada); 16 from Asia/SE Asia (China, Japan, Hong Kong, Singapore, Malaysia, Philippines, Thailand, Taiwan); 7 from Africa (South Africa, Zambia); 5 from Europe (Switzerland, Belgium, Netherlands); 4 from the Indian continent (Pakistan, Nepal); 4 from the United Kingdom; 2 from the Middle East (Israel, Dubai); and 3 records of unknown origin. Records specifically from humans are shown in Table 1. Table 1. Ticks taken directly from humans in New Zealand* Tick species (number of records) Country of origin Disease associations** Ixodes holocyclus (31) Australia Rickettsia australis; paralysis Amblyomma triguttatum triguttatum (5) Australia Coxiella burnetii Amblyomma (?) loculosum (1) Australia None reported Amblyomma spp. (4) Australia Ixodes tasmani (1) Australia R. australis; R. honei Ixodes spp. (1) Australia Haemaphysalis bancrofti (1) Australia None reported Bothriocroton hydrosauri (1) Australia R. honei Ixodidae (3) Australia Rhipicephalus sanguineus (1) PNG R.conorii; R .rickettsii (RMSF);CCHF; paralysis Dermacentor andersoni (1) USA RMSF;&nb

Summary

Abstract

Humans coming into New Zealand occasionally, and unwittingly, bring exotic ticks with them, either attached to their bodies or with luggage. Of the 172 available records for tick interception at New Zealands border, half can be attributed to human agency. Here, together with an outline of tick biology and ecology, we present evidence of at least 17 species of ticks being brought in by humans, with Australia, North America and Asia the most frequent countries of origin. Risks posed by some of the nine species of ticks already in New Zealand are briefly examined. Sites of attachment of ticks and associated symptoms where these have been recorded are presented. Diseases transmitted by ticks and most likely to be encountered by travellers are briefly discussed together with the most practical method of tick removal. A plea is made for practitioners to increase their awareness of the risks to New Zealands biosecurity and public health posed by ticks and to ensure that as many as possible of these unwelcome souvenirs are collected and passed on for identification.

Aim

Method

Results

Conclusion

Author Information

Allen C G Heath, Senior Scientist, AgResearch Ltd, National Centre for Biosecurity and Infectious Disease, Wallaceville, Upper Hutt; Scott Hardwick, Scientist, AgResearch Ltd., Lincoln Research Centre, Lincoln

Acknowledgements

We thank MAF Biosecurity NZ, various colleagues and general practitioners and laboratory personnel who provided ticks and data relating to infestations, especially Ricardo Palma and Rachel Cane and the late Bob Pilgrim. This work was carried out under the Better Border Biosecurity (B3) programme, funded by the Foundation for Research Science and Technology, with additional assistance from MAF Biosecurity New Zealand. We thank Jos 00e9 Derraik for reading and commenting on an earlier version of this paper and thanks to two anonymous referees for their comments. We also thank those who provided information on their tick infestations but wished to retain their anonymity.

Correspondence

Allen Heath, Senior Scientist, AgResearch Ltd, National Centre for Biosecurity and Infectious Disease, PO Box 40063, Wallaceville, Upper Hutt, New Zealand, 5140. Fax: +64 (0)4 5280355

Correspondence Email

allen.heath@agresearch.co.nz

Competing Interests

None

Heath ACG, Palma RL, Cane RP, Hardwick S Checklist of New Zealand ticks (Acari: Ixodidae, Argasidae). Zootaxa 2011 (in press)Sonenshine DE. Biology of ticks, volume 2. Oxford University Press, 1993.MAF Biosecurity New Zealand, Import Health Standards: http://www.biosecurity.govt.nz/enter/personal/pets updated 21 April 2010 [accessed 26 October 2010]Estrada-Pe 00f1a A, Jongjan F. Ticks feeding on humans: a review of records on human-biting Ixodoidea with special reference to pathogen transmission. Exp Appl Acarol 1999;23:685-715.Varma MRG. 1993. Ticks and mites (Acari), In: Medical insects and arachnids, Lane RP, Crosskey RW editors London, Chapman & Hall, 1993:597-658.Telford SR, Goethert HK. Emerging and emergent tick-borne infections, In: Bowman AS, Nuttall PA editors, Ticks, biology, disease and control. Cambridge University Press, 2008:344-76.Barboza P, Tarantola A, Lassel L, Mollet T, Quatresous I, Paquet C. Viroses 00e9mergentes en Asie du Sud-Est et dans le Pacifique. Med Mal Infect.2008;38:513-23.Labuda M, Nuttall PA. Viruses transmitted by ticks In: Bowman AS Nuttall PA, editors, Ticks Biology, Disease and Control, Cambridge, University Press, 2008:253-80.Looke DFM, Robson JMB. Infections in the returned traveler. Med J Aus 2002;177:212-19.Lederman ER, Weld LH, Elyazar IRF, von Sonneburg F, Loutan L, Schwartz E, Keystone JS. Dermatologic conditions of the ill returned traveler: an analysis from the GeoSentinel Surveillance Network. Int J Infect Dis 2008;12:593-602.Shaw MTM, Leggat PA, Weld LH, Williams ML, Cetron MS. Illness in returned travellers presenting at GeoSentinel sites in New Zealand. Aust NZ J Public Health 2003;27:82-86.OBrien BM. A practical approach to common skin problems in returning travellers. Travel Med Infect Dis 2009;7:125-46.Mackenzie JS, Williams DT. The zoonotic flaviviruses of southern, south-eastern and eastern Asia, and Australasia: the potential for emergent viruses. Zoonoses Public Health 2009;56:338-56.Dobler G. Zoonotic tick-borne flaviviruses. Vet Microbiol 2010;140:221-28.Statistics New Zealandhttp://www.stats.govt.nz/browse_for_stats/population/Migration/IntTravelAndMigration_HOTPJune2010/Commentary.aspxJune 2010 [accessed 26 October 2010]Parola P, Paddock CD, Raoult D. Tick-borne rickettsioses around the world: emerging diseases challenging old concepts. Clin Microbiol Rev 2005;18:719-56.Paddock CD. The science and fiction of emerging rickettsioses. Ann N Y Acad Sci 2009;1166:133-43.Graves S, Stenos J. Rickettsioses in Australia. Ann N Y Acad Sci 2009;1166:151-55.Hilbink F, Penrose M, Kovacova E, Kazar J. Q fever is absent from New Zealand. Int J Epidemiol 1993;22:945-49.Greenslade E, Beasley R, Jennings L, Woodward A, Weinstein P. Has Coxiella burnetii (Q fever) been introduced into New Zealand? Emerg Infect Dis 2003;9:138-40.Arricau-Bouvery N, Rodolakis A. Is Q fever an emerging or re-emerging zoonosis? Vet Res 2005;36:327-49.Heath ACG. Vector competence of Haemaphysalis longicornis with particular reference to blood parasites. Surveillance 2002;29 (4):12-14.Piesman J, Gern L. Lyme borreliosis in Europe and North America, Parasitology 2004;129:S191-S220.Olsen B, Duffy DC, Jaenson TGT, Oylfe A, Bonnedahl J, Bergstrom S. Transhemispheric exchange of Lyme disease spriochetes by seabirds. J Clin Microbiol 1995;3:3270-74.Russell RC. Vectors vs. humans in Australia - who is on top down under? An update on vector-borne disease and research on vectors in Australia. J Vector Ecol 1998;23:1-46.Port Macquarie News: (http://www.portnews.com.au/news/local/news/general/diagnosis-positive-tick-disease-is-here/1944198.aspx 17 September 2010 [accessed 26 October 2010]Ellis-Pegler R, Ingram J. Health advice for overseas travellers. Wellington: Ministry of Health, 1996.New Zealand Ministry of Foreign Affair and Trade http://www.safetravel.govt.nz/ updated 3 March 2010 [accessed 26 October 2010]Miles J. Infectious diseases: colonising the Pacific? Dunedin, University of Otago Press, 1997.Fairley R., Heath ACG. Exotic ticks intercepted in New Zealand since 1980. Surveillance 1997;24(1):21-22.Heath ACG. Exotic tick interceptions 1980-2000. Surveillance 2001:28(4):13-15.Loth L. Review of exotic tick interceptions in New Zealand since 1980. Surveillance 2005;32(3):7-9.New Zealand Ministry of Tourism statistics; http://www.tourismresearch.govt.nz/Morrissey T. Intelligence at the border. Biosecurity 2010;100:3Roberts FHS. Australian ticks. Melbourne, CSIRO, 1970.Waudby HP, Petit S, Weber D. Human perception and awareness of ticks in a South Australian rural community and implications for management of Amblyomma triguttatum triguttatum. Exp Appl Acarol. 2008;45:71-84.Sexton DJ, Dwyer B, Kemp R, Graves S. Spotted fever group rickettsial infections in Australia. Rev Infect Dis. 1991;13:876-86.Pearce RL, Grove DI. Tick infestation in soldiers who were bivouacked in the Perth region. Med J Aust. 1987 146:238-40Miller MK. Massive tick (Ixodes holocyclus) infestation with delayed facial-nerve palsy. Med J Aust. 2002;176:264-5.Sutherland SK. Ticks, In: Sutherland SK, editor, Australian animal toxins: the creatures, their toxins and care of the poisoned patient. Melbourne, Oxford University Press, 1983;299-315.Centers for Disease Control and Prevention, Department of Health and Human Services, USA;http://www.cdc.gov/ticks/diseases/ Updated September 2010 [accessed 26 October 2010]Mans BJ, Gothe R, Neitz WH. Tick toxins: perspectives on paralysis and other forms of toxicoses caused by ticks. In: Bowman AS, Nuttall PA, editors, Ticks, biology, disease and control, Cambridge University Press, 2008:108-26.Gratton-Smith PJ, Morris JG, Johnston HM, Yiannikas C, Malik R, Russell R, Ouvrier RA. Clinical and neurophysiological features of tick paralysis, Brain 1997;120:1975-87.Brown FT, Hamilton DL. Tick bite anaphylaxis in Australia. J Accid Emerg Med 1997;15:111-13.Rowe RS. 1980. Cattle tick infestation. N Z Med J 91, 472-473.Heath ACG. 1986. Interception of the brown dog tick, Rhipicephalus sanguineus infesting man. N Z Vet J 34,76-77.Humphery-Smith I, Cybinski DH. Health risks from tick-transmitted arboviruses on Australias Great Barrier Reef. Med J Aust. 1987;146:606-7.Humphery-Smith I, Cybinski DH, Moorhouse DE, Dale D. Arboviruses and zoonotic infections on the Great Barrier Reef and in the Coral Sea. Arbovirus Research in Australia, Proceedings 4th Symposium, 1986:209-17.Oxer DT, Ricardo CL. 1942. Notes on the biology, toxicity and breeding of Ixodes holocyclus (Neumann). Aust Vet J 18, 194-199.Sutherst RW, Moorhouse DE. 1971. Ixodes holocyclus larvae and scrub-itch- in south-east Queensland. Southeast Asian J Trop Med Public Health 2, 82-83.Moorhouse DE. 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