Journal of Infection (2008) 56, 83e98 www.elsevierhealth.com/journals/jinf REVIEW Human infections associated with wild birds Sotirios Tsiodras a,*,g, Theodoros Kelesidis b,g, Iosif Kelesidis b, Ulf Bauchinger c,f, Matthew E. Falagas d,e a University of Athens Medical School, 1 Rimini Street, Xaidari, 12462 Athens, Greece Beth Israel Deaconess Medical Center, Harvard University Medical School, Boston, MA, USA c University of Munich (LMU), Planegg-Martinsried, Germany d Alfa Institute of Biomedical Sciences, Athens, Greece e Department of Medicine, Tufts University School of Medicine, Boston, MA, USA f Mitrani Department of Desert Ecology, Ben-Gurion University of the Negev, Ben-Gurion, Israel b Accepted 1 November 2007 Available online 21 December 2007 KEYWORDS Communicable diseases; Avian infection; Wild birds; Infectious diseases; Influenza; Lyme disease; Arbovirus; West Nile encephalitis; Enteric infection; Antimicrobial resistance Summary Introduction: Wild birds and especially migratory species can become long-distance vectors for a wide range of microorganisms. The objective of the current paper is to summarize available literature on pathogens causing human disease that have been associated with wild bird species. Methods: A systematic literature search was performed to identify specific pathogens known to be associated with wild and migratory birds. The evidence for direct transmission of an avian borne pathogen to a human was assessed. Transmission to humans was classified as direct if there is published evidence for such transmission from the avian species to a person or indirect if the transmission requires a vector other than the avian species. Results: Several wild and migratory birds serve as reservoirs and/or mechanical vectors (simply carrying a pathogen or dispersing infected arthropod vectors) for numerous infectious agents. An association with transmission from birds to humans was identified for 10 pathogens. Wild birds including migratory species may play a significant role in the epidemiology of influenza A virus, arboviruses such as West Nile virus and enteric bacterial pathogens. Nevertheless only one case of direct transmission from wild birds to humans was found. Conclusion: The available evidence suggests wild birds play a limited role in human infectious diseases. Direct transmission of an infectious agent from wild birds to humans is rarely identified. Potential factors and mechanisms involved in the transmission of infectious agents from birds to humans need further elucidation. ª 2007 The British Infection Society. Published by Elsevier Ltd. All rights reserved. * Corresponding author. Tel.: þ30 210 5831989, þ30 6932 665820; fax: þ30 210 5326446. E-mail address: tsiodras@med.uoa.gr (S. Tsiodras). g The first two authors contributed equally to this work. 0163-4453/$30 ª 2007 The British Infection Society. Published by Elsevier Ltd. All rights reserved. doi:10.1016/j.jinf.2007.11.001 84 Introduction Free-living birds, including migratory species, can become long-distance vectors for a wide range of microorganisms that can be transmissible to humans.1 This creates the potential for establishment of novel foci of emerging or re-emerging communicable diseases along bird migration routes.2 Certain pathogens are more often isolated in migratory birds in comparison to other animal species3,4 and the potential for transport and dissemination of these pathogens by wild birds is of increasing public health concern stimulated by the recent spread of diseases like highly pathogenic Avian influenza A (HPAI H5N1 Asian lineage) and West Nile virus (WNV) infection.3,5 Avian influenza A (HPAI H5N1 Asian lineage) and West Nile virus infection, well known to affect birds for decades, have been recently observed to affect areas far away from the locations where they were originally identified, generating the hypothesis that migratory birds transported these pathogens to new geographical locations.6 However as is the case with the highly pathogenic avian influenza, scientific data do not always support such hypotheses.7 Several factors affecting wild bird species including migratory species such as increasing stress levels and crowding potentially promote infectious disease transmission among birds but available data supporting this are scarce or nonexistent. The objective of this paper is to summarize available literature on pathogens causing human disease that have been associated with wild birds including wild migratory bird species. Although wild bird borne infections can occur at any spatial scale, from very localized, to short and long distance, from an epidemiologic point of view the transmission of pathogens from wild birds to humans over a long distance is most important. Therefore, in the current manuscript we focused more on the role of wild migratory birds in the spread of certain pathogens. The paper focuses on available evidence of transmission of avian borne pathogens to humans. We speculated that such evidence would originate from enhanced animal and human surveillance and the application of advanced molecular diagnostic testing during the recent years. Furthermore, we attempted to identify factors potentially contributing to such transmission from the available body of science. Methods Two reviewers (TK and IK) independently performed the literature search. The following terms were used in searches of the PubMed database: ‘‘wild birds’’, ‘‘migratory birds’’, ‘‘infection’’, and specific pathogens known to be associated with wild and migratory birds e.g. ‘‘West Nile virus’’, ‘‘avian influenza’’, ‘‘influenza A’’, ‘‘Lyme disease’’ and ‘‘arbovirus’’. We also screened articles related to the initially identified publications to expand our data sources. Despite the availability of scientific data on this issue even before 19668,9 we focused in the modern area where molecular diagnostics might enhance our ability to study such interactions between birds and humans. Similar searches were conducted for each individual migratory S. Tsiodras et al. bird species identified through a list provided by the Royal Ornithological Society of Great Britain and World bird databases (Avibase World List).10,11 We also used the widely used Sibley and Monroe Classification for birds.12,13 To evaluate the role of recent diagnostic developments, we also performed an additional search of the literature by using the term polymerase chain reaction (PCR) and ‘‘migratory birds’’. Additional epidemiologic information for the identified pathogens-diseases was obtained from the websites of the United States Centers for Disease Control (CDC), World Health Organization (WHO), FAO, and OIE.14,15 Study selection and data extraction The role of wild and migratory birds in the transmission of an infectious disease to humans was discussed in consensus meetings where all authors participated. Transmission to humans was classified as direct if there was evidence for direct transmission of the pathogen from the avian species to humans through direct contact with an infected bird and genetic/serological evidence of the presence of a particular pathogen in both the avian species and humans. Transmission to humans was classified as indirect if there was evidence for transmission of the pathogen from the avian species to humans through indirect contact with an infected bird and genetic/serological evidence of the presence of the particular pathogen in both the avian species and humans. We considered indirect ways of transmission, those through contaminated water from feces of waterfowls and through vectors that are carried by wild birds such as mosquitoes and ticks (Table 1). Finally, we classified pathogens to be associated with a ‘‘theoretical risk for transmission’’ when in the literature there were reports that these pathogens were isolated both from humans and wild birds, using microbiological, genetic or serological methods, but there were no reports of actual direct/indirect transmission of these pathogens from wild birds to humans. Despite the lack of actual evidence in such cases, the risk exists in theory e.g. through ingestion of water contaminated from feces of wild birds or exposure to inanimate surfaces contaminated by bird secretions or droppings. Compiled relevant bird species data (with formal avian family names) are presented in the appendix. This appendix further includes data on pathogens that are borne by wild avian species that have not yet been associated with human infection in published reports. Results Evidence for direct transmission The systematic review of the literature review identified no real evidence for direct wild bird to human transmission with the only exception being the cluster of H5N1 human cases in Azerbaijan where the affected patients were plucking feathers from mute swans that had succumbed to H5N1 infection.16 Wild birds and human infections Table 1 85 Pathogens that have been reported to be indirectly transmitted from wild birds including migratory species to humans Microorganism(s) (I) Bacteria Chlamydiaceae Chlamydophila psittaci Enterobacteriaceae Escherichia coli Salmonella (enterica typhimurium) Mycobacteriaceae Mycobacterium (avium, ulcerans) Spirochaetaceae Borrelia burgdorferi sensu lato genomic species Reported transmission to human (indirect transmission) (n Z 10) Migratory bird species (formal family names for each bird species can be found in the appendix) Geographic area Ornithosis17e22 Egrets (Ardea Alba), grackles (Quiscalus), gulls (Larus), migratory waterfowl species (Anatidae), passerines (Passeriformes), pigeons (Columbidae), psittacine birds (Psittaciformes), raptors (North American raptors), shorebirds (North American shorebirds), wild ducks (Anatidae), and others Worldwide Bloody diarrhea [Vero cytotoxinproducing E. coli O157, Shiga toxin stx2fcontaining E. coli O128 strain)23,24]25,26 Salmonellosis (enteritis)27e30 Finches (Fringillidae), gulls (Larus), pigeons (Columbidae), sparrows (Passeridae), starlings (Sturnidae) Wild crows (Corvidae), ducks (Anatidae), gulls (Larus), passerines (Passeriformes), raptorial birds (North American raptors), songbirds (Passeriformes), terns (Sternidae), waterfowls (Anatidae) Worldwide Regarding M. avium it is generally believed and occasionally reported that man (especially immunocompromised, elderly) can contract the disease from birds, but this has not been fully clarified.31e33 Possible transmission of M. ulcerans to humans through contaminated water from feces of waterfowls (Anatidae)34 Lyme disease30,35e41 Crows (Corvidae), raptors (North American raptors), rooks (Corvus frugilegus), wild ducks (Anatidae), wild pigeons (Columbidae) Worldwide American Robins (Turdus migratorius), cardinals, songbirds (Passeriformes), sparrows (Passeridae), thrushes (Turdidae) and other ground foraging birds, waterfowl (Anatidae) North America, Europe Europe, South America, Asia Worldwide (II) Fungi Cryptococcus Yes (wild pigeons)42e46 Psittacine birds (Psittaciformes), starling (Sturnidae), wild pigeons (Columbidae) (III) Viruses Flaviviridae West Nile virus Yes3,30,47e49 North American shorebirds, common Africa Europe, grackles (Quiscalus quiscula), doves, Asia, America hawks, house finches (Carpodacus mexicanus), and house sparrows (Passer domesticus), songbirds (Passeriformes), raptors (North American raptors), owls (Strigidae), and various corvids (crows, jays, Corvidae) (continued on next page) 86 S. Tsiodras et al. Table 1 (continued) Microorganism(s) Reported transmission to human (indirect transmission) (n Z 10) Migratory bird species (formal family names for each bird species can be found in the appendix) Geographic area St. Louis encephalitis virus (SLEV) Yes3,49e51 America Western Equine Encephalitis virus (WEEV) Yes49 North American shorebirds, common grackles (Quiscalus), doves, hawks, house finches (Carpodacus mexicanus), and house sparrows (Passer domesticus), songbirds (Passeriformes), owls (Strigidae), and various corvids (crows, jays, magpies) North American shorebirds, quails (Coturnix) Orthomyxoviridae Influenza A virus To date, only domestic poultry are known to have played a major role in the transmission cycle of the H5N1 virus from animals to humans.52 However, there is also the potential contribution of other hosts like carnivores e.g cats to both virus transmission and adaptation to mammals.53,54 Dead or moribund cats were found to be infected with H5N1 virus soon after the virus was detected in wild birds in Germany.53 This suggests that H5N1 virus can be transmitted from wild birds to cats53 whereas in another report avian influenza A virus subtype H5N1 was transmitted to domestic cats by close contact with infected birds.54 However, there has been no documented case with wild migratory bird to human transmission although the theoretical risk exists.55 Serologic evidence of avian influenza infection in 1 duck hunter and 2 wildlife professionals with extensive histories of wild waterfowl (Anatidae) and game bird exposure has been reported.56 There is an association (not necessarily causal) between recreational contact with H5N1 contaminated water and the onset of confirmed human H5N1 disease in 3 cases.53,57,58 In one of these cases asymptomatic ducks may have shed virus into the pond.53 Possible direct transmission of highly pathogenic avian influenza in family cluster in Azerbaijan.16 Occupational exposure to avian species may increase veterinarians’ risk of avian influenza virus infection.59 Transmission can cause: Respiratory infection, keratoconjuctivitis, diarrhea, encephalitis30,60e66 Dabbling ducks (e.g common MallardAnas platyrhynchos), geese (Anserinae), gulls (Larus), swans (Cygninae), guillemots (Uria aalge), mountain hawk eagles (Spizaetus nipalensis) North American Bluewinged Teal (Spatula discors), shearwaters (Procellariidae), terns (Sternidae). Wild aquatic birds are regarded as the principal reservoir of influenza viruses, and migrating ducks (Anatidae) disseminate influenza viruses worldwide America Worldwide Wild birds and human infections Evidence for indirect transmission or a theoretical risk for transmission Although a large number of avian borne pathogens have been identified in the literature, we found relatively scarce evidence for indirect transmission of avian borne pathogens to humans (Table 1). Unfortunately, in the vast majority of the reports reviewed herein, data were unavailable to further characterize the way of transmission of certain pathogens beyond the stage of a speculative argument. This would be expected for zoonoses which usually require amplification in an animal species cycle before spill-over to humans. Nevertheless and based on our criteria several avian borne bacterial, fungal, viral pathogens could be indirectly transmitted or associated with a theoretical risk for transmission to humans (Table 1). We identified 58 such pathogens for which wild birds can serve as reservoirs, mechanical vectors, or both (Tables 1 and 2). However, the paucity of available data did not allow us to make the distinction whether the involved species serve as reservoir or vector in most of the cases. Scarce microbiological, serological and epidemiological data supported indirect transmission from wild birds to human for 10 of these pathogens (Table 1). Application of advanced molecular diagnostic testing during the recent years has led to the isolation of these microbial agents known to affect humans in birds. The examples include bacterial spp. like Escherichia coli,24,25 Borrelia Burgdorferi,37 Anaplasma phagocytophilum,87 Salmonella typhimurium,28 Campylobacter spp.,79 and Mycobacterium spp.,31e33 viruses like Influenza virus,56,60,61,64,65 West Nile virus,126 St. Louis encephalitis virus3,50,51 and Western Equine Encephalitis virus49 and fungi like Cryptococcus spp..43,44,46 These have been isolated from many wild birds using standard serological3,30,47,48,50,51,56,60,61,64,65,79 and microbiological techniques.28,31e33,37,43,44,46,79,126,127 Moreover vectors with the ability to carry pathogens have also been isolated from wild birds.3,37,85,87 For example, ornithophilic mosquitoes and ticks are the principal vectors of pathogens like West Nile virus in the Old World, and B. burgdorferi, respectively, and birds of several species, chiefly migrants, appear to be the major introductory or amplifying hosts of these vectors.3,37,85,87 Methods that have been used to confirm association of microbial agents isolated from wild birds with infection in humans include molecular methods like sequence analysis for Ehrlichia85 and Mycobacterium species,32,33 phylogenetic analysis,25 pulsed-field gel electrophoresis,26 polymerase chain reaction,26 immunomagnetic separation (IMS) for E. coli,25,26 serological methods for influenza virus56,59 and psittacosis,17 and epidemiological methods for Salmonella spp.,28,29 Borrelia spp.,36 West Nile virus,30,48,49,126 St. Louis encephalitis virus,49,51 and Western Equine Encephalitis virus.49 However, in most scientific literature, there is no detailed data regarding the detection and characterization of pathogens and their relation to wild birds. In most of the cases, it seems that wild birds serve as vectors of the pathogen. In these cases, the indirect role of wild birds in transmission of the infectious agents can be only speculated and the implicated pathogens are classified as having 87 the theoretical risk of transmission from wild birds to humans (Table 2). Twenty-one wild avian family species were identified that are reservoirs, mechanical vectors or both for infectious agents that may affect humans (Listed with their formal family names in the appendix according to the Sibley and Monroe Classification for birds). A short description of pathogens that may be transmitted from wild birds to humans is outlined below. Types of microorganisms carried by wild birds that could affect humans (indirect transmission or theoretical risk) Bacteria A range of bacterial pathogens affecting humans has been associated with wild and migratory birds. An indirect transmission to humans has been reported for some of these such as the enteric pathogens E. coli24 and Salmonella spp.28,29 Tick-borne pathogens such as Borrelia burgdorferi sensu lato species have been also associated with human infection from wild migratory birds.35e38,85,87 A theoretical risk for transmission to humans has been reported for other bacterial pathogens such as Yersinia spp.,76,128 Campylobacter jejuni77 and both cholera and non-cholera Vibrio spp.92 Fungi Yeasts and yeast-like fungi have been isolated from wild and migratory birds such as Candida spp.,129,130 and hyphomycetes e.g. Aspergillus spp., Microsporum spp., Trichophyton spp.,112 and cryptococci.43 A theoretical risk for transmission to humans exists but scientific data to support this are extremely scarce. Cryptococci that are quite ubiquitous in nature have been reported to be transmitted to humans indirectly from wild pigeons (Columbidae), occasionally causing clinical infection, especially in immunocompromised patients.42 Viruses Important viral species have been isolated from wild migratory birds and can affect humans indirectly including influenza A viruses,62,131 the West Nile virus (WNV),3,47 the St. Louis encephalitis virus (SLEV).3,50,51 Several other viral species can theoretically be transmitted from wild birds to humans (Table 2). Parasites Wild and migratory birds can disperse in nature a diverse number of protozoa such as Babesia and other haemoparasites. The potential for transmission exists for some parasitic species (Table 2). Factors potentially contributing in transmission The issue of the transmissibility of various pathogens from wild birds including migratory species to humans is fairly complex. Several factors determine the possibility of such a spread. Some factors relate to the affected species including the birds themselves (e.g. the avian species involved, susceptible local vertebrate recipients or Pathogens with theoretical risk for transmission (but no reports of actual direct/indirect transmission) from wild birds including migratory species to humans (I) Bacteria Gram-positive cocci Enterococcus Staphylococcus Gram-positive rods Clostridium perfringens Listeria monocytogenes Enterobacteriaceae Yersinia species Campylobacteraceae Campylobacter jejuni Helicobacter spp. Anaplasmataceae Anaplasma phagocytophilum Migratory bird species Geographic area Possible spread through polluted water67,68; transmission has been reported from other birds69e71 Ducks (Anatidae), seagulls (Larus), waterfowls (Anatidae) and other migratory birds such as quails (Coturnix) Ducks (Anatidae), mallards (Anas platyrhynchos), passerines (Passeriformes), seagulls (Larus), and other migratory birds including quails (Coturnix), raptors (North American raptors) Worldwide Crows (Corvidae), ducks (Anatidae), gulls(Larus), Pelicans (Pelecanus) and marine birds, raptors (North American raptors), shorebirds (North American shorebirds), waterfowls (Anatidae) Crows (corvus), gulls (Larus), rooks (Corvus frugilegus) and other migratory birds Crows (corvus), ducks (Anatidae), gulls (Larus), magpies, (Corvidae) pigeons (Columbidae), pheasants, starlings (Sturnidae), terns (Sternidae), wagtails (Motacilla), waterfowls (Anatidae) and other migratory species Europe, Asia Migrating ducks (Anatidae), passerine birds e.g. crows (corvus), pigeons (Columbidae) and seagulls (Larus), sparrows (Passeridae) Europe, North America, Asia Geese (Anserinae), gulls (Larus), passerines (Passeriformes), terns (Sternidae), various wild birds North America, Europe, Australia Geese (Anserinae), gulls (Larus) Worldwide Geese (Anserinae), seagulls (Larus), swans (Cygninae), wild ducks (Anatidae) Passerine birds (Passeriformes) American Robins (Turdus migratorius), robins, songbirds (Passeriformes) veery (Catharus fuscescens), American warbler Worldwide Possible through faecal pollution of environmental water samples72 Possible through accidental ingestion of contaminated water73; food-borne enteritis has been reported from non-migratory birds74 Possible through accidental ingestion of contaminated water75 Enteritis30,76 Intestinal campylobacteriosis.30,77,78 Whether waterfowl (Anatidae) have a role in the dissemination of Campylobacter spp. that results in increased human disease is likely to be elucidated through development and greater use of typing methods.79 Typing might allow links to be established between isolates of avian, environmental, and human origin.79 Enteritis (Helicobacter canadensis).80,81 Possible transmission of H. pylori by contaminated water from feces of waterfowls (Anatidae)82 Possible through faecal pollution of environmental water samples72,83 Possible through faecal pollution of environmental water samples e.g. gulls (Larus)84 Human granulocytic ehrlichiosis85e87 Worldwide America, Asia Worldwide North America, Europe, Asia S. Tsiodras et al. Other gram negative bacilli (Pseudomonas, Aeromonas, etc.) Anaerobic bacteria Potential for transmission to humans exists (n Z 50) 88 Table 2 Microorganism(s) Rickettsiaceae Coxiella burnetii Vibrionaceae Vibrio cholerae (II) Viruses Bunyaviridae Nairoviruses: CrimeanCongo haemorrhagic fever (CCHF) Coronaviridae Avian infectious bronchitis virus, other coronaviruses Flaviviridae Japanese encephalitis virus (JEV) Other flaviviruses Murray Valley encephalitis virus (MVEV), Usutu virus (USUV) Sindbis virus Tick-borne Encephalitis virus (TBE) Herpesviridae Anatid herpesvirus 1, (duck plague virus), Marek virus Paramyxoviridae Newcastle disease virus (NDV, avian parainfluenza virus 1, paramyxovirus-1) Tuberculosis.88 Possible transmission of mycobacterium from humans to birds has been reported through close contact between humans and pet birds but it is not known if humans can acquire the infection from birds.88 Possible through ticks 90,91 Green-winged macaw, psittacines (Psittaciformes)88,89 Pigeons (Columbidae) Europe, Asia Cholera, non-cholera Vibrio infections92,93 Wild aquatic birds (Anatidae), gulls (Larus) North America Possible transmission through ticks and transmission has been reported for other birds94,95 Crows (Corvidae), wild aquatic birds (Anatidae), passerines (Passeriformes), rooks, (Corvus frugilegus) Europe, Asia, Africa Serological evidence in humans exposed to birds has been reported96 Passerines (Passeriformes), pheasants (Phasianidae) Worldwide Yes97e99 Colonial ardeids (Ardeidae), herons (Ardeidae), marsh birds, quails (Coturnix) Blackbirds (Turdus merula), wading birds, crows and magpies (Corvidae) (Usutu virus), Pelecaniformes (MVE virus) Wild birds and human infections Mycobacterium species M. tuberculosis Worldwide Yes (MVEV)100,101 NR (USUV) Ockelbo disease,102,103 Pogosta disease,104 plus possible transmission to humans as migratory birds are hosts of mosquitoes which are vectors for these viruses Possible through ticks 105e108 Marek’s virus (transported by wild birds) has been associated with multiple sclerosis in humans.109,110 Serological evidence in humans exposed to migratory birds has been reported.96 Can cause self-limiting conjunctivitis as occupational exposure to affected poultry Blackbird (Turdus merula), carrion crow (Corvus corone), passerine birds (Passeriformes) wild grouse (Tetraonidae), wild ducks (Anatidae) Blackbirds (Turdus merula), sandpipers (Scolopacidae), wild mallards (Anas platyrhynchos), wild grouse (Tetraonidae), other wild birds Japanese quails (Coturnix coturnic japonica), passerines (Passeriformes), pigeons (Columbidae), raptors (North American raptors), wild anseriforms (Anatidae), geese (Anserinae), swans (Cygninae) Cormorants (Phalacrocoracidae), gulls (Larus), passerines (Passeriformes), pelicans (Pelecanus), raptors (North American raptors), waterfowls (Anatidae) Europe, America Europe, Asia, North America, and Africa Worldwide 89 (continued on next page) 90 Table 2 (continued) Microorganism(s) Potential for transmission to humans exists (n Z 50) Migratory bird species Geographic area Other Paramyxoviridae (pneumoviruses) NR Gulls (Larus), waterfowl (Anatidae) Europe, Africa, Asia Possible through faecal pollution of environmental water samples with wildfowl droppings111,112 Coots (Fulica), grebes (Podicipedidae), herring gulls (Larus argentatus), migratory ducks (Anatidae), owls (Strigidae), storks (Ciconiidae), swans (Cygninae) House-sparrows (Passer domesticus), seagulls (Laridae), starlings (Sturnidae) Wild geese (Anserinae), wild woodcocks (Scolopax) Worldwide Picornaviridae Egg drop syndrome virus Foot-and-mouth disease virus Reoviridae Avian rotavirus, orbivirus and other spp. Togaviridae Eastern (EEE ) and Western (WEE ) equine encephalitis viruses Venezuelan equine encephalitis virus (VEE) (III) Parasites Coccidia (Eimeria) Cryptosporidium Helminths parasites Sarcocystis NR but according to some studies birds do not have an important role in the transmission of enteroviruses113 Not reported but evidence for transmission to mammals111,114e116 Possible through mosquitoes that are vectors for these viruses117,118 Possible through mosquitoes that are vectors for these viruses 119,120 Possible through contamination with faecal material121 Has been reported for other non-migratory birds122 Possible food-borne through eating small water fish.123 Cercarial dermatitis (swimmer’s itch) due to exposure to marine schistosomes124 Possible through contaminated water125 Cliff swallows (Petrochelidon pyrrhonota), finches (Fringillidae), American Robins (Turdus migratorius, smaller species of Passeriformes, several trans-Gulf migrant starlings (Sturnidae), waterbirds (Anatidae) Nestling birds such as Cliff swallows, North American shorebirds, songbirds (Passeriformes), wild ducks (Anatidae) Europe Asia, Africa, Europe, America America South to Central America Cranes (Gruidae), owls (Strigidae), wild pigeons (Columbidae), waterfowls (Anatidae) Cranes (Gruidae), exotic seagulls (Larus), wild anseriforms: ducks (Anatidae), geese (Anserinae), swans (Cygninae) and wild birds (order Passeriformes, Phasianidae, Fringillidae, and Icteridae), waterfowl species (Anatidae) Gulls (Larus), ducks (Anatidae), passerines (Passeriformes), waterfowl species (Anatidae) North America, Asia, Africa America, Africa, Asia Cowbirds (Molothrus), exotic birds, mallards (Anas platyrhynchos), passerines (Passeriformes), wading birds, wild anseriforms (Anatidae), geese (Anserinae), swans (Cygninae) America, Africa, Europe Australia, Europe, Africa, Asia, America S. Tsiodras et al. Wild birds and human infections invertebrate vectors), others to the pathogen itself (e.g. stability of the agent in the environment), and lastly some factors relate to the environment (e.g. temperature, humidity). Studies of certain pathogens like influenza virus illustrate the interaction of factors that limit the transmission and subsequent establishment of an infection in a novel host species and may help us in understanding how and why some pathogens become capable of crossing host species barriers.132 Factors relating to the implicated pathogen and the affected species Pathogens associated with wild and migratory birds may be transmitted to humans via several routes. Generation of contaminated aerosols by waterfowl flocks may result in respiratory infections through inhalation of dust or fine water droplets generated from infected bird feces or respiratory secretions in the environment (e.g. Newcastle Disease or chlamydiosis).30 Birds can contaminate water with feces, nasal discharges, and respiratory secretions (e.g. influenza A virus, Enterobacteriaceae) resulting in a waterborne human infection after direct contact with aquatic environments.30 Recently, the European CDC concluded that the bathing risk in the case of waters contaminated with the H5N1 virus cannot be excluded and should be assessed on a case by case basis even though the chance of such an event is highly unlikely.133 Food-borne infections may result after consumption of infected carcasses of wild birds or raw or undercooked blood, organs, or meat, e.g., WNV, avian influenza A (H5N1), M. avium, Clostridium spp., Sarcocystis, Frenkelia.52,63,134 Infections may lastly result after direct contact with the skin, feathers, external lesions or droppings of infected wild birds (e.g. avian pox, WNV encephalitis, H5N1, mycoplasmal conjunctivitis). A major source of wild birdehuman contact is hunting and the cleaning of killed birds. Often birds are field-dressed by hunters with minimal protection bringing them in contact with blood, organs and feces.30 Serologic evidence of avian influenza infection in hunters and wildlife professionals has been reported.56 In addition, occupational exposure to avian species (e.g veterinarians) may increase risk of infections like avian influenza virus infection. Indirect infection may occur through the same routes if wild birds transmit the infection to domestic animals, e.g. poultry or via exposure to inanimate surfaces contaminated by bird secretions or droppings. Transfer of infected material can happen with shoes, clothing or other inanimate objects. Wild birds when serving as reservoirs exhibit multiplication of the pathogen within their organism. Aggregations of bird species that occur during certain periods within the avian annual cycle may enable transmission of pathogens between individuals. Extreme examples for such aggregations can be found at moulting and staging areas of eared grebes Podiceps nigricollis,135,136 at roosting sites for European starlings Sturnus vulgaris, at landbridges between continents (e.g. Gibraltar, Bosporus) widely used by soaring and gliding species like larger birds of prey and white storks Ciconia ciconia and at breeding sites of many seabirds. In terms of numbers, the vast amount of migratory birds do migrate solitarily in ‘broad front’ and therefore do not encounter an increased risk of pathogen transmission, while 91 some species travel hundreds to thousands of kilometres from their breeding grounds and re-fuel at distinct stopover sites.137 These ‘‘staging areas’’ provide the opportunity for close intermingling of species that are otherwise widely separated during the major part of the year.35,138 Thus, the theoretical opportunity for exchange of pathogens is increased among avian species, which make use of the same stopover sites. In such instances duration and concentration of the agent in the blood or the gastrointestinal tract of migrating birds are important for the subsequent infection of another competent vector that feeds or gets exposed in crowding situations or during stopover e.g. a tick. Several studies have recorded infections e.g. B. burgdorferi and human granulocytic ehrlichiosis (HGE) in ticks removed from birds.36,37,87 Ticks commonly infest a wide range of avian species, especially, sparrows (Passeridae), thrushes and other ground foraging birds.30,36,37,139,140 Although a wide range of tick species has been reported to parasitize wild birds, Ixodes spp. are the most likely ones to carry infections (e.g. B. burgdorferi) especially in Europe and North America. Ixodid ticks often attach to hosts for 24e 48 hours while acquiring a blood meal. In tick-borne viruses, bacteria, and protozoa, the infectious larval or nymphal tick may remain attached to the body of a migratory bird for several days and then deposited during migration in a new geographic area. During migration, there is sufficient time for some birds to travel hundreds or even a few thousand miles before ticks complete feeding and drop off. Even if these birds have small tick burdens, their large numbers could result in substantial contributions to local tick populations in coastal areas.40 There is even evidence of transhemispheric exchange of spirochete-infected ticks by seabirds indicating the capacity for wild birds to carry infected ticks for long distances.141 Moreover, birds can carry infections in their bloodstream which is introduced to local population of ticks at other sites. Therefore, birds play an important role not only in maintaining infections such as B. burgdorferi sensu lato in areas of endemicity, in addition some of them, through their migration, also play a role by spreading ticks within and between continents.36,139,142,143 Exposure to tick-borne diseases is primarily peridomestic, so the contribution to tick related human infection of avian ticks relative to mammalian ticks around dwellings is critical.38 Birds that are implicated in peridomestic transmission of tick related infections to humans, especially in North America, include American robins (Turdus migratorius), northern cardinals (Cardinalis cardinalis), and song sparrows (Melospiza melodia) that frequently use backyard environments and some of which are commonly seen at bird feeders. Therefore, they are likely to drop engorged larvae in peridomestic environments like lawns and gardens,40 where ticks are less common than in woods and at wood edges but more likely to encounter people.38,144 Even though the survival of nymphs is low in open habitats, the contribution of birds to human infection in the peridomestic environment could be substantial and deserves further study.40 An additional factor is the physiologic stress that wild migratory birds suffer with migration, a risk factor for immunosuppression and increased susceptibility to infectious diseases. Avian species may exhibit an increased susceptibility to certain pathogens (e.g. West Nile virus) compared to other vertebrate groups.3,4 Changes and 92 adaptations occur in migratory birds during long-distance migration.63 For some birds, the stress of migration can lead to reactivation of otherwise latent infections.145 West Nile virus was isolated from migrating birds that were under migratory stress.146 However, an opposing argument is that infected migratory birds could not survive long-distance travel; thus their role in transmitting communicable diseases is of less importance.147 For example, in the case of avian influenza most outbreaks in wild birds seem to reflect local acquisition of infection from a contaminated source, followed by rapid death nearby.148 There is only limited evidence that some wild birds can carry the virus asymptomatically, and no evidence from wild bird outbreaks that they have done so over long distances during seasonal migration.148 Understanding the balance between the changes and adaptations that occur in migratory birds during longdistance migration is important to comprehend susceptibility of certain migratory birds to develop infections. Similar factors e.g. age and bird gender may in addition influence migratory patterns leading to spread of diseases in novel geographical areas.3 Factors relating to the implicated pathogen and the environment Migrants of most bird species in the New World seldom use the same stopover sites on northward, spring migration as they do on southward, fall migration. This is because migration routes are determined by complex interactions of environmental factors such as direction of prevailing winds, weather patterns, location of available food resources and geographical barriers (e.g. large bodies of water, deserts and mountains). These factors seldom combine to favour the same route in different seasons.3 Seasonality is a significant factor influencing both, wild birds (wild resident and migratory species) and other vectors e.g. mosquitoes, ticks leading to changes in transmission dynamics.149e151 For mosquitoes, a spring population peak in Europe and North America occurs during the spring migration of birds.146e148 The effect of seasonality in the flyway patterns of major migratory birds was observed for certain diseases such as West Nile virus encephalitis. The incidence of West Nile virus disease is seasonal in the temperate zones of North America, Europe, and the Mediterranean Basin, with peak activity from July through October.152 Both avian and human infection rates drop to near zero as winter approaches and mosquitoes become dormant.153 Season is important for some non-vector-borne pathogens, as well. For example, influenza A viruses remain infectious in water at lower ambient temperatures and at the same time major congregations of migratory waterfowl occur, increasing the likelihood of transmission among birds. Furthermore, numerous bird species (e.g. crows and gulls) are attracted to untreated sewage, garbage dumps, manure, and other sources of enteric pathogens that can then be transmitted to humans. These areas should be appropriately covered and not open to the access of wild migratory birds. Migratory bird flyways and transmission Long-distance migration is one of the most demanding activities in the animal world and several studies demonstrate S. Tsiodras et al. that such prolonged, intense exercise leads to immunosuppression exacerbating the possibility of spreading infections. On the other hand, infected symptomatic wild birds may act as vectors over shorter distances.154 Understanding bird migration, avian migration patterns and infectious diseases of birds would be useful in helping to predict future outbreaks of infections due to emerging zoonotic pathogens and can provide important information that could explain the pattern of spread of certain infectious agents. Numerous variations in flyways exist. For some ocean migratory wild birds, a nomadic wandering that can appear random is probably related to poorly understood weather or ocean conditions.155,156 Major migratory flyways, especially between continents are known to be used by migratory birds when commuting between breeding and wintering areas and vice versa. Nevertheless, these flyways are only used by a fraction of the existing species on the move, predominately by waterfowl and soaring and gliding migrants like large raptors and storks which aggregate and follow fairly easily defined routes. The complex overlapping of major flyways and the lack of information on migratory species potentially involved in the spread of disease make simple association of wild migratory flyways with outbreaks of certain infections extremely difficult despite the significant amount of literature on the subject. For example, in Alaska, there is a notable overlap between the Pacific and East Asia/ Australasia flyways through which scientists believe avianflu-infected migrating birds, such as the bar-tailed godwit (Limosa lapponica), dunlin (Calidris alpina), and red knot (Calidris canutus), will transfer the Asian strains of H5N1 influenza virus to North American birds over the next few months14 although this was not confirmed in a recent study.157 On the other hand, other more local migratory bird routes have been described in association with West Nile virus outbreaks.3 Societal factors Furthermore, societal factors like captivation of wild birds in zoos and importation and sale of wild birds as pets should also be considered as important factors which can enhance the spread of pathogens from wild birds to humans. Cryptosporidium has been reported to be transmitted from some non-migratory birds in zoos to humans.122 A theoretical similar risk for avian influenza exists as avian influenza was recently isolated from a wild swan in the Dresden zoo in Germany.157 Similar risk can be encountered in bird parks since outbreaks of infections related to birds like psittacosis have occurred.17 Finally, the international trade of exotic pet birds carrying influenza A viruses enhances the risk of worldwide dissemination of potentially virulent influenza A virus and may pose a serious health threat to humans.158 Limitations of the current literature review There are several limitations of this work and clearly further work is necessary. Some of the identified agents are quite ubiquitous in the environment raising the question about how to quantify the additional impact wild resident Wild birds and human infections and migratory birds may have on transmission. There is still scientific debate over the actual role migratory birds might play in the transmission of certain communicable diseases. In support of this argument we did not find any evidence for direct transmission from wild and migratory birds to humans for any of the identified pathogens the only exception being the cluster of H5N1 human cases in Azerbaijan.16 In addition, in many cases, there was no further available information that would allow further elucidation of the real epidemiological role played by wild birds in the ecology of the considered infections, especially in underdeveloped countries. Many reports do not exactly clarify how the birds are implicated in the transmission of these infections and in the majority of cases this transmission could not be established by adequate scientific methods. Thus, in many of the reports reviewed herein, there were no data regarding serologic assays or molecular diagnostic techniques used to detect and characterize pathogens and identify birds as vectors of disease. In these cases only associations of these infections with migratory birds could be made (Table 2). The evidence reviewed herein suggests that many pathogens can infect multiple host bird species and that these pathogens in theory could be responsible for emerging infectious disease outbreaks in humans and wildlife. However, the ecologic and evolutionary factors that constrain or facilitate such emergences are poorly understood. In the literature, a different terminology is used to describe the interaction between hosts, including wild birds, and pathogens. Terms such as multihost pathogens, reservoir hosts, and spill-overs are frequently used, but often such different terms are used to describe the same phenomenon. There is a need for a single, standardised comprehensive framework that characterizes disease outcomes based on biologically meaningful processes. An example of such conceptual framework is based on the pathogen’s betweenand within-species transmission rates and can be used to describe possible configurations of a multihostepathogen community.159 In particular, the much-overused terms reservoir and spill-over can be seen to have explicit definitions, depending on whether the pathogen can be sustained within the target host population.159 However, the paucity of available published data did not allow us to determine whether the involved species of certain wild birds serve as reservoir or spill-over. Finally, only few studies have reviewed the role of migratory birds in transmission of all different infections and these studies remain descriptive.112 Migratory birds cannot be blamed for recurrent outbreaks at the same geographical location over subsequent years unless there is in an introduction of the pathogen to known or novel avian or other animal reservoir hosts and vectors. Furthermore, for some viruses that are considered to be transmitted by wild migratory birds (e.g. West Nile virus), duration of high levels of viremia for most species tested has been found to be limited and usually less than 24 hours. However, exceptions to that rule exist. The house sparrow (Passer domesticus) has demonstrated WNV viremia of sufficient duration to indicate its ability to serve as a competent host for WNV.3 Furthermore, other modes of transmission such as the import of infected products may be of equal importance in 93 the spread of diseases like avian influenza and scientists are still debating the evidence of the role of migratory birds in the wide geographical spread of the influenza A (H5N1) virus. Highly pathogenic avian influenza viruses have been isolated rarely from wild birds and, apart from a single case in common terns in South Africa,160 when they have, it has usually been in the vicinity of outbreaks of highly pathogenic avian influenza virus in poultry or geographically and chronologically close to known outbreaks in poultry. In fact the de novo generation of highly pathogenic avian influenza virus strains (restricted to subtypes H5 and H7) so far has been described to have occurred only in domestic poultry and the occurrence of highly pathogenic avian Influenza viruses in wild birds is most likely the result from spill-overs from the poultry population. Another important limitation is that there is no way to predict whether the comprehensive lists presented in this paper may expand in the near future. Moreover, the fact that a lot of the pathogens carried by wild and migratory birds that are presented in Table 2 have not been associated with human infection does not mean that these pathogens cannot cause human infection through routes presented for other pathogens in the same table. Future directions Identifying links between environmental factors and infectious disease risk is essential to understanding how human-induced environmental changes will affect the dynamics of human and wildlife diseases. Studying large wetland areas, and by extension, intact wetland bird communities, may represent a valuable ecosystem-based approach for controlling infections caused by migratory birds including WNV.161 Recent evaluations suggesting links between high biodiversity among wild birds and reduced vector-borne disease risk, such as WNV, may lead to a better understanding of distribution patterns of such diseases.48 Recent findings on the origin of the WNV infections suggest a single species to act as a super spreader and the transmission of WNV appears in new light.162 These recent findings demonstrate imposingly how important detailed studies on contact rates between vectors and host species are and how careful interpretations need to be made before drawing any conclusions. Estimation of the infection rate of wild bird populations with human pathogens or with other vectors carrying pathogens is clearly an indicated future challenge required to judge the possibilities of bird to human transmission of pathogens. The same accounts for the transmission between and within bird species. Recent investigations indicate the influence of social and sexual behaviours and their seasonal components on intra-specific transmission,163,164 while the inter-specific transmission rate remains speculative. Birds are considered to show behavioural changes due to pathogen infection, which will considerably influence transmission rates.163 Furthermore, accurate data on the speed and direction of migratory birds may enable us to predict the timing of bird migration in more detail; this will assist in monitoring the risk of infections that may be caused by wild birds. While this knowledge is available for larger bird species due to the use of satellite tracking, only limited data are available on the 94 individual level for some North American songbirds with the use of radio-telemetry tracking.165 Producing maps depicting the ecology of the vectors including mosquitoes and ticks ecology in combination with maps of migratory routes of wild birds along with access to real time climatic data could be the key for developing a real time early warning system for forecasting vector-borne disease outbreaks.166 The spatial and temporal pattern of migration of wild birds as well the spatial distribution throughout the annual cycle can provide further insight. Application of stable isotope analysis has already resulted in new insights where bird populations spend the time between the seasonally reoccurring breeding events,167 a knowledge which can be of great importance for future predictability of disease outbreaks. Human medicine often does not delve deeply into the role of animals in the transmission of zoonotic agents and veterinary medicine does not cover the clinical aspects of human disease. However, to effectively and completely cover the area of infections associated with wild birds would require involvement of both physicians and veterinarians especially those dealing with avian species.168 Unfortunately, one recent study demonstrated that communication between physicians and veterinarians about zoonotic diseases is largely absent.168 Therefore, one important factor that could potentially explain the paucity of available data regarding the transmission of pathogens from wild birds to humans could be the lack of communication between physicians and ornithologists. To most effectively decrease the risk of infections associated with wild birds, the public health and animal health sectors must collaborate in developing strategies to decrease human exposure to pathogens carried by wild birds. An effective public educational campaign could also put in perspective and clarify myths and realities about the risk of acquiring infections associated with wild birds. Activities near geographical areas with extensive wild bird activity really carry minimal risk especially if people take personal protective measures for high risk activities such as handling dead wild waterfowl. Normal behaviour that complies with general hygienic standards should suffice. Conclusions We attempted to summarize the published scientific evidence regarding the direct and indirect roles of wild birds in transmission of certain infections to humans. Although we could not fully define this role and it appears that further research is necessary, several conclusions can be made. First, there is no real evidence for direct wild birdehuman transmission besides rare examples occurring under exceptional circumstances. Several human infections can theoretically be transmitted from wild and migratory birds although the scientific base for most of the associations remains speculative. These findings are expected for zoonoses, which usually require the amplification in an animal species cycle before spill-over to humans. Wild and migrant birds are most important in seeding pathogens into these amplification systems. This explains why most of the association with transmission from bird to human may only occur indirectly. On the other hand, there is strong S. Tsiodras et al. evidence for the dispersal of pathogens to new geographical locations by migrating birds but it is largely unknown how this will affect transmission to humans. The recent emergence of infections like West Nile virus and influenza A in various parts of the world is a prominent example of how rapidly and widely a migratory bird associated disease can spread. The potential factors and mechanisms involved in the transmission of such infectious agents from birds to humans need further elucidation. An in-depth comprehension of avian migration routes as well as further research using advanced molecular testing of the prevalence, pathogenesis, and clinical associations of several pathogens that are transmitted to humans from the various migratory bird species would lead to a better understanding of the transmission dynamics of diseases carried by avian species helping to predict future outbreaks of relevant human infections. Conflict of interest None. Supplementary data Supplementary data associated with this article can be found, in the online version, at doi:10.1016/j.jinf.2007. 11.001. References 1. Nuttall PA. Viruses, bacteria, and fungi of birds. In: Clayton DH, Moore J, editors. Hosteparasite evolution. Oxford, UK: University Press; 1997. p. 271e302. 2. National Institute of Allergy and Infectious Diseases. 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