Migrating birds and tickborne encephalitis virus.During spring and autumn 2001, we screened 13,260 migrating birds at Ottenby Bird Observatory A bird observatory is a centre for the study of bird migration and bird populations. They are usually focused on local birds, but may also include interest in far flung areas. , Sweden, and found 3.4% were infested in·fest tr.v. in·fest·ed, in·fest·ing, in·fests 1. To inhabit or overrun in numbers or quantities large enough to be harmful, threatening, or obnoxious: with ticks. Four birds, each a different passerine passerine Any perching bird. All passerines belong to the largest order of birds, Passeriformes, and have feet specialized for holding onto a horizontal branch (perching). The passerine foot has three forward-directed toes and one backward-directed toe. species, carried tickborne encephalitis encephalitis (ĕnsĕf'əlī`təs), general term used to describe a diffuse inflammation of the brain and spinal cord, usually of viral origin, often transmitted by mosquitoes, in contrast to a bacterial infection of the meninges virus (TBEV TBEV Tick-Borne Encephalitis Virus )-infected ticks (Ixodes ricinus). Migrating birds may play a role in the geographic dispersal of TBEVinfected ticks. ********** Tickborne encephalitis is a viral zoonotic disease Noun 1. zoonotic disease - an animal disease that can be transmitted to humans zoonosis animal disease - a disease that typically does not affect human beings caused by the tickborne encephalitis flavivirus (TBEV). There are 3 subtypes of TBEV: the European subtype (programming) subtype - If S is a subtype of T then an expression of type S may be used anywhere that one of type T can and an implicit type conversion will be applied to convert it to type T. (TBEV-Eu, transmitted by Ixodes ricinus ticks) and the Siberian and Far-Eastern subtypes (TBEV-Sib and TBEV-FE, transmitted by I. persulcatus ticks) (1-3). Geographic distribution of TBEV subtypes largely follows that of their tick hosts: I. ricinus (Europe) and I. persulcatus (from Far East to the Baltic countries) (4). In Latvia and Estonia, the distribution of both tick species overlaps, and all 3 TBEV subtypes cocirculate in Latvia (3). Thus, a range expansion of a tick species could result in spreading a TBEV subtype to new areas. Small rodents are thought to be the main amplifying hosts, although wild ungulates ungulates, ungulata animals with hooves; cattle, sheep, goat, pig, horse and many wild and other domesticated species. contribute indirectly by providing blood meals for adult ticks, thereby maintaining the vector populations necessary for virus transmission. In addition to mammals, I. ricinus ticks take blood meals from birds, which has led to speculation that birds could disperse TBEV-infected ticks during migration and start new TBE foci. In this study, we document the occurrence of TBEV-infected ticks in migrating birds. The Study Fieldwork was conducted during 2001 at Ottenby Bird Observatory, located on the southernmost tip of Oland, a large island off the southeast coast of Sweden (56[degrees]12' N, 16[degrees]24' E; Figure). Throughout spring (March 25-June 15) and autumn (July 1-November 15) migration, observatory personnel captured and screened birds for ticks, except during 8 days when an excessive number of trapped birds made complete monitoring impossible. Each captured bird was identified by species and age and was banded. For bird species with TBEV-infected ticks, local banding and recovery records from 1946 to the present were used to determine recruitment and wintering areas. [FIGURE OMITTED] Tick screening comprised rapid visual assessment for the presence of any ticks on bare body parts, especially around the eyes and beak of each bird. All ticks were removed by forceps, placed separately into snap-lid tubes, frozen and stored at -70[degrees]C, and then analyzed with a dissecting dis·sect tr.v. dis·sect·ed, dis·sect·ing, dis·sects 1. To cut apart or separate (tissue), especially for anatomical study. 2. microscope to identify species and development stage. A Puregene RNA RNA: see nucleic acid. RNA in full ribonucleic acid One of the two main types of nucleic acid (the other being DNA), which functions in cellular protein synthesis in all living cells and replaces DNA as the carrier of genetic isolation protocol adopted for 100-10,000 cells (Gentra Systems, Minneapolis, MN, USA) individually homogenized ho·mog·e·nize v. ho·mog·e·nized, ho·mog·e·niz·ing, ho·mog·e·niz·es v.tr. 1. To make homogeneous. 2. a. To reduce to particles and disperse throughout a fluid. b. each tick and extracted RNA, according to the manufacturer's instructions. The RNA pellet was resolved in 25 [micro]L DNA DNA: see nucleic acid. DNA or deoxyribonucleic acid One of two types of nucleic acid (the other is RNA); a complex organic compound found in all living cells and many viruses. It is the chemical substance of genes. hydration hydration /hy·dra·tion/ (hi-dra´shun) the absorption of or combination with water. hy·dra·tion n. 1. The addition of water to a chemical molecule without hydrolysis. 2. buffer and stored at -70[degrees]C until further analysis. Samples were pooled 10 by 10 (5 [micro]L from each individual extract) and analyzed by a nested reverse transcription reverse transcription n. The process by which DNA is synthesized from an RNA template. (RT)-PCR targeting the 5'-terminal noncoding region (5) for the initial detection of TBEV RNA. Briefly, the RTPCR RTPCR Reverse Transcriptase Polymerase Chain Reaction was performed in 25-[micro]L reaction volumes containing 1 x EZ buffer, 0.3 mmol of each deoxyribonucleotide deoxyribonucleotide /de·oxy·ri·bo·nu·cleo·tide/ (-noo´kle-o-tid) a nucleotide having a purine or pyrimidine base bonded to deoxyribose, which in turn is bonded to a phosphate group. dNTP), 2.5 U rTth DNA polymerase DNA polymerase /DNA po·lym·er·ase/ (pah-lim´er-as) any of various enzymes catalyzing the template-directed incorporation of deoxyribonucleotides into a DNA chain, particularly one using a DNA template. , 2.5 mmol Mn[(OAc).sub.2] (all reagents provided from Perkin Elmer, Branchburg, N J, USA), 25 pmol of each primer (Ppl and Pml), 25 U Rnasine (Gibco, Paisley, Scotland, UK), and the target viral RNA. The reaction was performed in a GeneAmp 9700 thermal cycler (Applied Biosystems, Foster City, CA, USA) programmed to incubate incubate /in·cu·bate/ (in´ku-bat) 1. to subject to or to undergo incubation. 2. material that has undergone incubation. in·cu·bate v. 1. 45 min at 60[degrees]C for RT and 2 min at 94[degrees]C for denaturation denaturation, term used to describe the loss of native, higher-order structure of protein molecules in solution. Most globular proteins exhibit complicated three-dimensional folding described as secondary, tertiary, and quarternary structures. as initial steps, followed by 40 cycles of 30 s at 94[degrees]C and 30 s at 66[degrees]C. The final extension was for 5 min at 66[degrees]C. Negative and positive controls were included in each PCR PCR polymerase chain reaction. PCR abbr. polymerase chain reaction Polymerase chain reaction (PCR) run. A second amplification step was conducted with 2 [micro]L of the first amplification products. The total reaction volume of 25 [micro]L included lx PCR buffer II, 1.5 mmol MgC[l.sub.2], 0.2 mmol each of dNTP, 0.625 U AmpliTaq Gold polymerase (Perkin Elmer), and 25 pmol of each internal primer (Pp2 and Pm2). After a pre-incubation step of 9 min at 95[degrees]C, the reaction was continued by 30 cycles of 15 s at 94[degrees]C and 30 s at 65[degrees]C and ended with an elongation step of 10 min at 72[degrees]C. Samples from positive pools were rerun re·run n. The act or an instance of rebroadcasting a recorded movie or a recorded television performance. tr.v. re·ran , re·run, re·run·ning, re·runs To present a rerun of. using individual samples with the nested PCR described above. During the study period, 1,155 ticks were collected from 447 (3.4%) of 13,260 screened birds (Table). Nearly all ticks (1,130) were reliably identified as I. ricinus. Seven nymphs showed characters resembling I. lividus, but these and 19 other ticks were rather poorly preserved, making identification uncertain. Frequencies of the various tick life stages were as follows: larvae Larvae, in Roman religion Larvae: see lemures. (53.4%), nymphs (45.1%), and adults (0.6%). The mean infestation infestation /in·fes·ta·tion/ (-fes-ta´shun) parasitic attack or subsistence on the skin and/or its appendages, as by insects, mites, or ticks; sometimes used to denote parasitic invasion of the organs and tissues, as by helminths. rate (0.086 immature ticks per examined bird, 2.6 immature ticks per infested bird) was unevenly distributed among bird species, with tick infestation in only 37 of>100 investigated species. Ground-foraging birds carried [approximately equal to]80% of all detected ticks and made up 71.3% of all infested birds (Table). A few ticks were also found on granivorous granivorous feeding on grain. bird species, e.g., siskins, finches, sparrows, and some insectivorous insectivorous eating insects to the extent that they are significant as a contributor to the patient's diet. songbirds, particularly among Sylvia and Acrocephalus warblers that forage in reed beds or dense stands of herbaceous plants (Table). The number of detected ticks per infested bird was usually in the range of 1-5 ticks, but 2 birds, a song thrush thrush, in medicine thrush, in medicine, infection caused by the fungus Candida albicans, manifested by white, slightly raised patches on the mucous membrane of the tongue, mouth, and throat. (Turdus philomelos) and a European robin (Erithacus rubecula), carried 41 and 39 ticks, respectively. After initial screening of pools and rerunning individual samples from PCR-positive pools, we detected 6 TBEV-positive samples: 4 tick nymphs and 2 larvae. One larva larva, in zoology larva, independent, immature animal that undergoes a profound change, or metamorphosis, to assume the typical adult form. Larvae occur in almost all of the animal phyla; because most are tiny or microscopic, they are rarely seen. was collected from a juvenile tree pipit (Anthus trivialis), 1 nymph nymph, in Greek mythology nymph (nĭmf), in Greek mythology, female divinity associated with various natural objects. It is uncertain whether they were immortal or merely long-lived. There was an infinite variety of nymphs. each from a song thrush and juvenile redstart redstart, common name for an Old World thrush of the genus Phoenicurus, family Turdidae. A small, slender-legged songbird, it is found in woodlands, parks, and heaths. The European redstart, P. (Phoenicurusphoenicurus), and 2 nymphs and 1 larva from a juvenile European robin. All TBEV-infected ticks were collected from birds during the autumn migration. Despite repeated trials, we were unable to obtain readable sequence data from the positive samples and could not identify the TBEV strains by subtype. Conclusions Our study found that some ticks attached to birds carried TBEV. However, the frequency of TBEV among such ticks was less than the frequency of Borrelia burgdorferi Borrelia burg·dor·fe·ri n. A spirochete causing Lyme disease in humans. Borrelia burgdorferi The spirochete agent of Lyme disease, which contains several outer membrane proteins and a highly immunogenic flagellar senso lato from similar datasets (6-8). Analyses of banding recovery data for the 4 bird species with TBEV-infected ticks indicate an eastern recruitment area coinciding with TBE-endemic areas in Fennoscandia and western Russia (Figure). TBEV has been isolated, or serologically indicated, from several bird species, especially anatids and gallinaceous birds, and most often from Eastern Europe or Russia (9). However, little is known about the capability of birds to function as reservoirs of TBEV, and small rodents remain the most important reservoirs of the virus. The fact that we found 2 I. ricinus larvae infected with TBEV could indicate that these birds may be reservoirs, because these larvae did not feed before attaching themselves to the birds. However, nonviremic transmission between ticks cofeeding on the same host has been shown to occur with TBEV (10) and other arboviruses arboviruses (ar´bōvī´r  sz),n. (11,12), and we did not look for viremia viremia /vi·re·mia/ (vi-re´me-ah) the presence of viruses in the blood. vi·re·mi·a n. The presence of viruses in the bloodstream. in the tick-infested birds. The migration of birds through Scandinavia during spring and fall involves several hundred million birds. Although the tick infestation rate per bird was not great in our study, and TBEV-infected ticks were only a small fraction of all ticks, the vast numbers of migrating birds do increase the probabilities for geographic spread of ticks and TBEV, in particular for TBEV-Eu, because I. ricinus predominated in our sample. Our data add to the growing body of evidence showing that migratory birds can disperse ticks infected with medically important pathogens (6, 7,10,13). Acknowledgments We thank staff and volunteers at Ottenby Bird Observatory for assistance with collecting ticks. This work was supported by the Swedish Medical Research Council (07922) and the Swedish Council for Forestry and Agricultural Research (grant no. 23.0161). This is contribution no. 217 from Ottenby Bird Observatory. Dr Waldenstrom is assistant professor at the Section for Zoonotic Zoonotic A disease which can be spread from animals to humans. Mentioned in: Zoonosis Ecology and Epidemiology, Kalmar University, Sweden. He has a broad interest in birdborne zoonotic infections from ornithologic or·ni·thol·o·gy n. The branch of zoology that deals with the study of birds. or  ni·tho·log and
epidemiologic perspectives.
References (1.) Ecker M, Allison SL, Meixner T, Heinz FX. Sequence analysis and genetic classification of tick-borne encephalitis viruses tick-borne encephalitis virus n. An arbovirus of the genus Flavivirus that occurs in two subtypes, Central European and Eastern, causing two forms of encephalitis; it is transmitted by ticks. from Europe and Asia. J Gen Virol. 1999;80:179-85. (2.) Mavtchoutko V, Vene S, Haglund M, Forsgren M, Duks A, Kalnina V, et al. Characterization of tick-borne encephalitis virus from Latvia. J Med Virol. 2000;60:216-22. (3.) Lundkvist A, Vene S, Golovljova l, Mavtchoutko V, Forsgren M, Kalnina V, et al. Characterization of tick-borue encephalitis virus from Latvia: evidence for co-circulation of tree distinct subtypes. J Med Viroi. 2001;65:730-5. (4.) Monath TP, Heinz FX. Flaviviruses. In: Fields BN, Knipe DM, Howley PM, editors. Fields virology virology, study of viruses and their role in disease. Many viruses, such as animal RNA viruses and viruses that infect bacteria, or bacteriophages, have become useful laboratory tools in genetic studies and in work on the cellular metabolic control of gene expression , 3rd ed. Philadelphia: Lippincot-Raven Publishers; 1996. p. 961-1034. (5.) Schrader C, Stiss J. A nested RT-PCR RT-PCR reverse transcriptase-polymerase chain reaction. See PCR1. for detection of tick-borne encephalitis virus (TBEV) in ticks in natural foci. Zentralbl Bakteriol. 1999;289:319-28. (6.) Comstedt P, Bergstrom S, Olsen B, Garpmo U, Marjavaara L, Mejlon H, et al. Migratory passerine birds as reservoirs of Lyme borreliosis Lyme borreliosis Another name for Lyme disease. Mentioned in: Lyme Disease in Europe. Emerg Infect Dis. 2006;12:1087-95. (7.) Olsen B, Jaenson TGT TGT Target TGT Ticket Granting Ticket (Windows 2000 Kerberos security) TGT Target Corp (stock symbol) TGT Turbine Gas Temperature TGT TDRSS Ground Terminal TGT Tank Gunnery Trainer TGT Target Tracker , Bergstrom S. Prevalence of Borrelia burgdorferi sensu lato-infected ticks on migrating birds. Appl Environ Microbiol. 1995;61:3082-7. (8.) Marie-Ange1e P, Lommano E, Humair PF, Douet V, Rais O, Schaad M, et al. Prevalence of Borrelia Borrelia A genus of spirochetes that have a unique genome composed of a linear chromosome and numerous linear and circular plasmids. Borreliae are motile, helical organisms with 4–30 uneven, irregular coils, and are 5–25 micrometers long and 0. burgdotferi senso lato in ticks collected form migratory birds in Switzerland. Appl Environ Microbiol. 2006;72:976-9. (9.) Hubalek Z. Pathogenic microorganisms associated with free-living birds (a review). Acta Sc Nat Brno. 1994;28:1-74. (10.) Labuda M, Nuttal PA, Kozuch O, Eleckova E, Williams T, Zuffova E, et al. Non-viraemic transmission of tick-borne encephalitis virus: a mechanism for arbovirus arbovirus Any of a large group of viruses that develop in arthropods (chiefly mosquitoes and ticks). The name derives from “arthropod-borne virus.” The spheroidal virus particle is encased in a fatty membrane and contains RNA; it causes no apparent harm to the survival in nature. Experentia. 1993;49:802-5. (11.) Jones LD, Davies CR, Steele GM, Nuttal PA. A novel mode of arbovirus transmission involving a nonviremic host. Science. 1987;237:775-7. (12.) Norman R, Ross D, Laurenson MK, Hudson PJ. The role of non-viraemic transmission on the persistence and dynamics of a tick borne virus--Louping ill in red grouse grouse, common name for a game bird of the colder parts of the Northern Hemisphere. There are about 18 species. Grouse are henlike terrestrial birds, protectively plumaged in shades of red, brown, and gray. (Lagopus lagopus scoticus) and mountain hares (Lepus timidus). J Math Biol. 2004;48:119-34. (13.) Bjoersdorff A, Bergstrom S, Massung RF, Haemig PD, Olsen B. Ehrlichia-infected ticks on migrating birds. Emerg Infect Dis. 2001;7:877-9. Address for correspondence: Jonas Waldenstrom, Kalmar University, Barlastgatan 11 Kalmar SE-391 82, Sweden; email: jonas.waldenstrom@ hik.se Jonas Waldenstrom, * ([dagger]) Ake Lundkvist, ([double dagger]) Kerstin I. Falk, ([double dagger]) Ulf Garpmo, * Sven Bergstrom, ([section]) Gunnel Lindegren, ([double dagger]) Anders Sjostedt, ([section]) Hans Mejlon, ([paragraph]) Thord Fransson, (#) Paul D. Haemig, * and Bjorn Olsen * ([paragraph]) * Kalmar University, Kalmar, Sweden; ([dagger]) Lund University, Lund, Sweden; ([double dagger]) Karolinska Institute, Solan, Sweden; ([section]) Umea University, Umea Sweden; ([paragraph]) Uppsala University, Uppsala, Sweden; and (#) Swedish Museum of Natural History The Swedish Museum of Natural History (in Swedish Naturhistoriska riksmuseet, literally, the National Museum of Natural History), in Stockholm, is one of two major museums of natural history in Sweden, the other one being located in Gothenburg. , Stockholm, Sweden
Table. Bird species infested with ticks during the spring and autumn
migration periods
Spring
Infesta-
tion
rate
(ticks/
Scientific No. No. infested
name Common name infested ticks bird)
Accipiter Eurasian - - -
nisus sparrowhawk
Acrocephalus Marsh warbler 1 1 1.0
palustris
Acrocephalus European reed - - -
scirpaceus warbler
Alauda Eurasian - - -
arvensis skylark
Anthus Tree pipit 1 1 1.0
trivialis
Carduelis Common linnet 1 1 1.0
cannabina
Carduelis European 6 6 1.0
chloris greenfinch
Carduelis Common redpoll - - -
flammea
Carduelis Eurasian 1 1 1.0
spinus siskin
Carpodacus Common - - -
erythrinus rosefinch
Certhia Eurasian - - -
familiaris treecreeper
Dendrocopos Great spotted - - -
major woodpecker
Emberiza Common reed - - -
schoeniclus bunting
Erithacus European 35 58 1.7
rubecula robin
Fringilla Common 1 1 1.0
coelebs chaffinch
Hippolais Icterine - - -
icterina warbler
Lanius Red-backed - - -
collurio shrike
Luscinia Thrush 2 5 2.5
luscinia nightingale
Luscinia Bluethroat 3 5 1.7
svecica
Parus Eurasian 2 3 1.5
caeruleus blue tit
Parus major Great tit 2 2 1.0
Phoenicurus Common 3 6 2.0
phoenicurus redstart
Phylloscopus Wood warbler - - -
sibilatrix
Phylloscopus Willow warbler 3 3 1.0
trochilus
Prunella Dunnock 2 6 3.0
modularis
Pyrrhula Eurasian - - -
pyrrhula bullfinch
Regulus Goldcrest - - -
regulus
Sturnus Common - - -
vulgaris starling
Sylvia Blackcap 1 2 2.0
atricapilla
Sylvia borin Garden warbler - - -
Sylvia Common 6 13 2.2
communis whitethroat
Sylvia curruca Lesser 2 4 2.0
whitethroat
Sylvia nisoria Barred warbler 2 3 1.5
Troglodytes Winter wren 7 16 2.3
troglodytes
Turdus iliacus Redwing 8 17 2.1
Turdus merula Common 24 86 3.6
blackbird
Turdus Song thrush 7 12 1.7
philomelos
_Turdus pilaris Fieldfare 1 4_ 4.0-
Total 121 256
Autumn
Infesta-
tion
rate
(ticks/
Scientific No. No. infested
name Common name infested ticks bird)
Accipiter Eurasian 1 2 2.0
nisus sparrowhawk
Acrocephalus Marsh warbler - - -
palustris
Acrocephalus European reed 1 1 1.0
scirpaceus warbler
Alauda Eurasian 1 6 6.0
arvensis skylark
Anthus Tree pipit 10 28 2.8
trivialis
Carduelis Common linnet - - -
cannabina
Carduelis European 1 1 1.0
chloris greenfinch
Carduelis Common redpoll 1 1 1.0
flammea
Carduelis Eurasian - - -
spinus siskin
Carpodacus Common 1 1 1.0
erythrinus rosefinch
Certhia Eurasian 2 2 1.0
familiaris treecreeper
Dendrocopos Great spotted 1 8 8.0
major woodpecker
Emberiza Common reed 1 1 1.0
schoeniclus bunting
Erithacus European robin 153 404 2.6
rubecula
Fringilla Common 1 8 8.0
coelebs chaffinch
Hippolais Icterine 2 15 7.5
icterina warbler
Lanius Red-backed 2 7 3.5
collurio shrike
Luscinia Thrush 2 4 2.0
luscinia nightingale
Luscinia Bluethroat 2 3 1.5
svecica
Parus Eurasian 4 11 2.8
caeruleus blue tit
Parus major Great tit 18 34 1.9
Phoenicurus Common 9 18 2.0
phoenicurus redstart
Phylloscopus Wood warbler 1 1 1.0
sibilatrix
Phylloscopus Willow warbler 16 18 1.1
trochilus
Prunella Dunnock 2 3 1.5
modularis
Pyrrhula Eurasian 5 8 1.6
pyrrhula bullfinch
Regulus Goldcrest 1 1 1.0
regulus
Sturnus Common 10 19 1.9
vulgaris starling
Sylvia Blackcap 6 6 1.0
atricapilla
Sylvia borin Garden warbler 1 1 1.0
Sylvia Common 12 33 2.8
communis whitethroat
Sylvia curruca Lesser 6 7 1.2
whitethroat
Sylvia nisoria Barred warbler 1 1 1.0
Troglodytes Winter wren 11 19 1.7
troglodytes
Turdus iliacus Redwing 2 5 2.5
Turdus merula Common 20 89 4.4
blackbird
Turdus Song thrush 18 131 7.3
philomelos
Turdus pilaris Fieldfare 2 2 -1
Total 326 899
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