Ehrlichia-infected ticks on migrating birds. (Dispatches).During the spring of 1996, an estimated 581,395 Ehrlichia-infected ticks were imported into Sweden by migrating birds. Ehrlichia gene sequences found in ticks collected from these migrating birds were identical to those of granulocytic granulocytic pertaining to granulocytes. granulocytic leukemia see myelocytic leukemia. granulocytic sarcoma extramedullary growth of multiple, focal granulocytic neoplasm. They may be neutrophilic or eosinophilic. ehrlichiosis found in domestic animals and humans in Sweden. These findings support the idea that birds may play a role in dispersing Ehrlichia. ********** The genus Ehrlichia contains several species of intracellular bacteria capable of causing clinical disease in humans and animals. Ehrlichiosis caused by Ehrlichia of the Ehrlichia phagocytophila genogroup has been diagnosed in horses, dogs, and cats in Sweden, as well as in cattle and sheep (1). Cases of ehrlichiosis have been reported among humans in Scandinavia (2), and in Sweden, Ehrlichia have been detected in the tick Ixodes ricinus(3). A common behavior of migrating birds is to feed and rest at stopover sites along their routes (4,5). At these sites, ticks and other ectoparasites may attach, and later detach along the migration route or in breeding areas. New foci of tick-borne diseases can be established in this way (6,7). Several investigations in Europe and the Middle East have examined the role of birds as carriers of ticks infected with tick-associated arboviruses arboviruses (ar´bōvī´r  sz),n. and the Lyme borreliosis Lyme borreliosis Another name for Lyme disease. Mentioned in: Lyme Disease agent, 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 sensu lato (7). However, the involvement of birds in the ecology and epidemiology of ehrlichiosis has not yet been studied. The Study Our investigation was designed to determine the frequency of Ehrlichia-infected ticks on migrating birds in Sweden and estimate the number of Ehrlichia-infected ticks being imported and exported by these birds. Ticks were collected from migratory 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. birds at a stopover site in southern Sweden (east coast of Oland), identified, and checked for the presence of Ehrlichia by polymerase chain reaction polymerase chain reaction (pŏl`ĭmərās') (PCR), laboratory process in which a particular DNA segment from a mixture of DNA chains is rapidly replicated, producing a large, readily analyzed sample of a piece of DNA; the process is (PCR PCR polymerase chain reaction. PCR abbr. polymerase chain reaction Polymerase chain reaction (PCR) ). To determine if different genomic species of Ehrlichia could be found in bird-borne ticks and indirectly in the birds, all Ehrlichia-positive PCR products were further subjected to DNA sequencing DNA sequencing The determination of the sequence of nucleotides in a sample of DNA. analysis. A total of 3,054 birds (1,204 in the spring and 1,850 in the fall) of 56 species were caught and examined for ticks. One hundred sixty-five Adj. 1. one hundred sixty-five - being five more than one hundred sixty 165, clxv cardinal - being or denoting a numerical quantity but not order; "cardinal numbers" ticks, all I. ricinus, were collected from 73 birds of 18 species (Table), for a tick 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. frequency of 2.4% (73/3,054) and a relative density of 0.054 ticks per bird (165/3,054). Fifty-one larvae Larvae, in Roman religion Larvae: see lemures. , 112 nymphs, and 2 adult females of I. ricinus were found (Table), suggesting that nymphs are more common than larvae on birds and that adult I. ricinus rarely feed on birds. Ehrlichia 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. was detected in none of the 51 larvae, in 8.0% (9/112) of the nymphs, and in none of the adult ticks. Ehrlichia DNA was detected in 8.9% (7/79) of the nymphs in the spring and 6.1% (2/33) in autumn. Ehrlichia 16SrRNA gene sequences in the nine positive nymphs were analyzed by DNA sequencing. The gene sequences (base positions 20-570 corresponding to base numbering for the U.S. human granulocytic ehrlichiosis human granulocytic ehrlichiosis: see ehrlichiosis. (HGE HGE hemorrhagic gastroenteritis. ) agent 16S rDNA; GenBank Accession Number Accession number may mean:
Conclusions Every spring, approximately 100 million birds migrate through Sweden, importing large numbers of potentially infectious ectoparasites. If the frequency of infected ticks is assumed to be similar to that in this study (7 Ehrlichia-infected ticks on 1,204 birds), 581,395 Ehrlichia-infected ticks were imported into Sweden by birds during the spring migration of 1996. The bird species we found carrying Ehrlichia-infected ticks (Table) breed in FennoScandia and arrived from wintering grounds in continental Europe Continental Europe, also referred to as mainland Europe or simply the Continent, is the continent of Europe, explicitly excluding European islands and, at times, peninsulas. , North Africa, and sub-Saharan Africa. During the fall migration, the frequency was lower (2 Ehrlichia-infected ticks found on 1,850 birds). However, even if the same number of birds migrated in the fall as in the spring, an estimated 108,108 Ehrlicha-infected ticks were exported from Sweden that fall by the birds. These figures support previous studies indicating that migratory birds are an important component in the dispersal of ticks infected with medically important pathogens (8). Only one species of tick (I. ricinus) was recorded in this study. This species is the main vector of B. burgdorferi sensu lato, E. phagocytophila, and tick-borne encephalitis virus 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. , both in Sweden and the rest of western and central Europe Central Europe is the region lying between the variously and vaguely defined areas of Eastern and Western Europe. In addition, Northern, Southern and Southeastern Europe may variously delimit or overlap into Central Europe. . The facts that a large number of birds are 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 this tick and that the Ehrlichia 16S rRNA gene sequences found in these ticks are identical to the gene sequences found in HGE patients in Sweden, Slovenia, and the USA suggest that birds may play an important role in the dispersal of I. ricinus infected with Ehrlichia and may contribute to the distribution of granulocytic ehrlichiosis (9). We found no I. ricinus larvae infected with Ehrlichia, which may suggest that birds are incompetent reservoirs of Ehrlichia but act as carriers of infected ticks. In this way, avian transport of Ehrlichia might differ from that of B. burgdorferi sensu lato. In the latter disease, birds not only carry infected ticks of all stages but can also carry latent infections 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. that can be reactivated by the stress of migration (10). However, the potential of a vertebrate vertebrate, any animal having a backbone or spinal column. Verbrates can be traced back to the Silurian period. In the adults of nearly all forms the backbone consists of a series of vertebrae. All vertebrates belong to the subphylum Vertebrata of the phylum Chordata. to function as a tick host and a reservoir for Ehrlichia depends on many factors, including the host's density in the tick habitat, the degree of contact between the potential tick vector and the host, and its infectivity. Therefore, the question of whether birds act as reservoirs of Ehrlichia has not yet been conclusively answered, and additional studies of various bird host species should be conducted over longer time spans than our study. Moreover, the reservoir competence of birds should be studied by isolation or detection of Ehrlichia after natural or experimental infection. The apparent increase of granulocytic ehrlichiosis in animals and humans during the last few decades may be the result of several factors, such as increased awareness of this disease and the distribution of reservoirs, vectors, and host animals. Whether passerine birds have affected this increase has not yet been conclusively demonstrated. However, our data suggest that birds are important in the dispersal of Ehrlichia.
Table. Migrating birds carrying Ixodes ricinus ticks and the
frequency of infection with Ehrlichia sp. in bird-borne ticks,
Sweden, 1996
Ehrlichia
DNA
detected
by PCR of
ticks
examined
Bird species (a) No. of birds
infested/
no. examined (%) No. of Larvae
ticks
Starling 1/10 (10) 1
(Sturnus vulgaris)
Dunnock 1/33 (3) 1
(Prunella modularis)
Reed Warbler 1/5 (20) 1
(Acrocephalus scirpaceus)
Icterine Warbler 1/12 (8) 1 0/1
(Hippolais icterina)
Garden Warbler (Sylvia borin) 2/79 (2.5) 2 0/1
Blackcap (S. atricapilla) 3/26 (11.5) 3 0/1
Whitethroat (S. communis) 1/29 (3.4) 1 0/1
Greenish Warbler 1/1 (100) 1 0/1
(Phylloscopus trochiloides)
Willow Warbler (P. trochilus) 3/1,025 (2.9) 4 0/4
Goldcrest (Regulus regulus) 1/892 (0.1) 1
Pied Flycatcher 1/22 (4.5) 1
(Ficedula hypoleuca)
Collared Flycatcher 1/2 (50) 1
(F. albicollis)
Redstart 7/76 (9.2) 28 0/11
(Phoenicurus phoenicurus)
Robin (Erithacus rubecula) 33/655 (5) 54 0/14
Thrush Nightingale 5/27 (18.5) 22 0/8
(Luscinia luscinia)
Blackbird (Turdus merula) 5/41 (12.2) 27 0/7
Song Thrush 4/24 (16.7) 14 0/2
(T. philomelus)
Bullfinch 2/27 (7.4) 2
(Pyrrhula pyrrhula)
Total 73/2,986 (2.4) 165 0/51
Ehrlichia
DNA
detected
by PCR of
ticks
examined
Bird species (a) No. of birds
infested/
no. examined (%) No. of Nymphs
ticks
Starling 1/10 (10) 1
(Sturnus vulgaris)
Dunnock 1/33 (3) 1 0/1
(Prunella modularis)
Reed Warbler 1/5 (20) 1 0/1
(Acrocephalus scirpaceus)
Icterine Warbler 1/12 (8) 1
(Hippolais icterina)
Garden Warbler (Sylvia borin) 2/79 (2.5) 2 0/1
Blackcap (S. atricapilla) 3/26 (11.5) 3 1/2
Whitethroat (S. communis) 1/29 (3.4) 1
Greenish Warbler 1/1 (100) 1
(Phylloscopus trochiloides)
Willow Warbler (P. trochilus) 3/1,025 (2.9) 4
Goldcrest (Regulus regulus) 1/892 (0.1) 1 0/1
Pied Flycatcher 1/22 (4.5) 1 0/1
(Ficedula hypoleuca)
Collared Flycatcher 1/2 (50) 1 0/1
(F. albicollis)
Redstart 7/76 (9.2) 28 1/17
(Phoenicurus phoenicurus)
Robin (Erithacus rubecula) 33/655 (5) 54 3/40 (b)
Thrush Nightingale 5/27 (18.5) 22 2/14
(Luscinia luscinia)
Blackbird (Turdus merula) 5/41 (12.2) 27 1/19 (c)
Song Thrush 4/24 (16.7) 14 1/12
(T. philomelus)
Bullfinch 2/27 (7.4) 2 0/2
(Pyrrhula pyrrhula)
Total 73/2,986 (2.4) 165 9/112
Ehrlichia
DNA
detected
by PCR of
ticks
examined
Bird species (a) No. of birds
infested/
no. examined (%) No. of Adults
ticks
Starling 1/10 (10) 1 0/1
(Sturnus vulgaris)
Dunnock 1/33 (3) 1
(Prunella modularis)
Reed Warbler 1/5 (20) 1
(Acrocephalus scirpaceus)
Icterine Warbler 1/12 (8) 1
(Hippolais icterina)
Garden Warbler (Sylvia borin) 2/79 (2.5) 2
Blackcap (S. atricapilla) 3/26 (11.5) 3
Whitethroat (S. communis) 1/29 (3.4) 1
Greenish Warbler 1/1 (100) 1
(Phylloscopus trochiloides)
Willow Warbler (P. trochilus) 3/1,025 (2.9) 4
Goldcrest (Regulus regulus) 1/892 (0.1) 1
Pied Flycatcher 1/22 (4.5) 1
(Ficedula hypoleuca)
Collared Flycatcher 1/2 (50) 1
(F. albicollis)
Redstart 7/76 (9.2) 28
(Phoenicurus phoenicurus)
Robin (Erithacus rubecula) 33/655 (5) 54
Thrush Nightingale 5/27 (18.5) 22
(Luscinia luscinia)
Blackbird (Turdus merula) 5/41 (12.2) 27 0/1
Song Thrush 4/24 (16.7) 14
(T. philomelus)
Bullfinch 2/27 (7.4) 2
(Pyrrhula pyrrhula)
Total 73/2,986 (2.4) 165 0/2
(a) Bird species sampled that did not carry ticks are not listed.
(b) One of these infected ticks was collected in the autumn.
(c) This infected tick was collected in the autumn.
Acknowledgments We thank Christian Cederroth for collecting ticks from the birds and Eva Olsson Engvall for valuable advice. This study was supported by the Swedish Medical Research Council (07922), the Swedish Council for Forestry and Agricultural Research (23.0161), the Swedish Natural Science Research Council, and the J.C. and Seth M. Kempes Memory Foundation. References (1.) Bjoersdorff A, Svendenius L, Owens JH, Massung RF. Feline granulocytic ehrlichiosis--a report of a new clinical entity and characterisation of the infectious agent infectious agent Pathogen, see there . J Small Anim Pract 1999;40:20-4. (2.) Karlsson U, Bjoersdorff A, Massung RF, Christensson B. Human granulocytic ehrlichiosis--a clinical case in Sweden. Scand J Infect Dis 2001;33:73-4. (3.) von Stedingk LV, Gurtelschmid M, Hanson HS, Gustafson R, Dotevall L, Engvall EO, et al. The human granulocytic ehrlichiosis (HGE) agent in Swedish ticks. Clin Microbiol Infect 1997;3:573-4. (4.) Alerstam T. Bird migration. Cambridge: Cambridge University Press Cambridge University Press (known colloquially as CUP) is a publisher given a Royal Charter by Henry VIII in 1534, and one of the two privileged presses (the other being Oxford University Press). ; 1990. (5.) Rappole JH. The ecology of migrating birds: a neotropical perspective. Washington: Smithsonian Institution Smithsonian Institution, research and education center, at Washington, D.C.; founded 1846 under terms of the will of James Smithson of London, who in 1829 bequeathed his fortune to the United States to create an establishment for the "increase and diffusion of Press; 1995. (6.) Anderson JF, Johnson RC, Magnarelli LA, Hyde FW. Involvement of birds in the epidemiology of the Lyme disease Lyme disease, a nonfatal bacterial infection that causes symptoms ranging from fever and headache to a painful swelling of the joints. The first American case of Lyme's characteristic rash was documented in 1970 and the disease was first identified in a cluster at agent Borrelia burgdorferi. Infect Immun 1986;51:394-6. (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.) Olsen B, Jaenson TGT, Noppa L, Bunikis J, Bergstrom S. A Lyme borreliosis cycle in seabirds and Ixodes uriae ticks. Nature 1993;362:340-2. (9.) etrovec M, Furlan SL, Zupanc TA, Strle F, Brouqui P, Roux Roux , Pierre Paul Émile 1853-1933. French bacteriologist. His work with the diphtheria bacillus led to the development of antitoxins to neutralize pathogenic toxins. V, et al. Human disease in Europe caused by a granulocytic Ehrlichia species. J Clin Microbiol 1997;35:1556-9. (10.) Gylfe A, Bergstrom S, Lundstrom J, Olsen B. Reactivation reactivation to become active after a period of quiescence or, as in bacterial and viral infections, latency. cross reactivation of Borrelia infection in birds. Nature 2000;403:724. Anneli Bjoersdorff, * ([dagger]) Sven Bergstrom, ([double dagger double dagger n. A reference mark (  ) used in printing and writing. Also called diesis.Noun 1. ]) Robert F. Massung, ([section]) Paul D. Haemig * ([double dagger]), Bjorn Olsen * ([double dagger]) * Kalmar County Hospital, Kalmar, Sweden; ([dagger]) Lund University Lund University has 7 faculties, with additional campuses in the cities of Malmö and Helsingborg, with a total of over 42,500 people studying in 50 different programmes and 800 separate courses. , Lund, Sweden; ([double dagger]) Umea University, Umea, Sweden; and ([section]) Centers for Disease Control and Prevention Centers for Disease Control and Prevention (CDC), agency of the U.S. Public Health Service since 1973, with headquarters in Atlanta; it was established in 1946 as the Communicable Disease Center. , Atlanta, Georgia, USA Dr. Bjoersdorff is a consultant in medical microbiology Medical microbiology is a branch of microbiology which deals with the study of microorganisms including bacteria, viruses, fungi and parasites which are of medical importance and are capable of causing diseases in human beings. in the Department of Clinical Microbiology Clinical microbiology The adaptation of microbiological techniques to the study of the etiological agents of infectious disease. Clinical microbiologists determine the nature of infectious disease and test the ability of various antibiotics to inhibit or kill and at the Research Center for Zoonotic Zoonotic A disease which can be spread from animals to humans. Mentioned in: Zoonosis Ecology and Epidemiology, Kalmar, Sweden. Address for correspondence: Bjorn Olsen, Research Center for Zoonotic Ecology and Epidemiology, Department of Infectious Diseases infectious diseases: see communicable diseases. , Kalmar County Hospital, SE-391 85 Kalmar, Sweden; fax: 46 90-13 30-06; e-mail: Bjornol@ltkalmar.se |
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