Evidence of the role of free-living birds as disseminators of Salmonella spp.

Evidências das aves de vida livre como transmissoras de Salmonella spp.

Antonio Jackson Forte Beleza William Cardoso Maciel Elisângela de Souza Lopes Átilla Holanda de Albuquerque Arianne Silva Carreira Carlos Henrique Guedes Nogueira Jéssica de Melo Bandeira Ruben Horn Vasconcelos Régis Siqueira de Castro Teixeira About the authors

ABSTRACT

This study aimed to review aspects of Salmonella spp. in free-living birds and their potential as disseminators for domestic animals, man, and the environment. Isolation of Salmonella spp. have been reported in several species of wild birds from Passeridae and Fringillidae, among other avian families, captured in countries of North America and Europe, where Salmonella ser. Typhimurium is the most frequently reported serotype. The presence of pathogens, including Salmonella, may be influenced by several factors, such as diet, environment, exposure to antibiotics, infection by pathogenic organisms and migration patterns. Researches with wild birds that live in urbanized environment are important, considering that birds may participate in the transmission of zoonotic pathogens, which are more prevalent in cities due to the human activity. Based on the information collected, this article concludes that wild birds are still important disseminators of pathogens in several geographic regions and may affect man, domestic animals, and other birds.

KEYWORDS
salmonellosis; wild birds; zoonosis

RESUMO

O objetivo deste estudo foi realizar uma revisão acerca da Salmonella spp. em aves de vida livre e o potencial delas como disseminadores para animais domésticos, homem e meio ambiente. Casos na literatura relatando Salmonella spp. têm sido descritos em diversas espécies de aves silvestres da família Passeridae e Fringilidae em países da América do Norte e Europa, sendo Salmonella ser. Typhimurium o sorotipo relatado mais frequentemente. A presença de patógenos como Salmonella spp. pode ser influenciada por fatores como dieta, ambiente onde vive, contaminação por antibióticos, infecção por organismos patogênicos e padrões de migração. Pesquisas envolvendo as aves silvestres que vivem em ambiente urbanizado são importantes, pois as aves podem possibilitar a transmissão de patógenos zoonóticos que têm maior prevalência em áreas urbanas devido a mecanismos de ação humana. Com base nas informações coletadas, conclui-se que as aves silvestres continuam sendo importantes na disseminação de patógenos em diversas regiões geográficas, podendo afetar o homem, animais domésticos e outras aves silvestres.

PALAVRAS-CHAVE
salmonelose; aves selvagens; zoonose

INTRODUCTION

Infectious diseases, including emerging infectious diseases, are a great threat to wildlife, animal production and human population (DASZAK et al., 2000DASZAK, P.; CUNNINGHAM, A.A.; HYATT, A.D. Emerging Infectious Diseases of Wildlife--Threats to Biodiversity and Human Health. Science, Washington, v.287, n.5452, p.443-449, 2000. https://doi.org/10.1126/science.287.5452.443
https://doi.org/10.1126/science.287.5452...
). However, episodes of populational decrease as a consequence of these diseases in wild birds often lack proper documentation due to the scarce knowledge on emerging pathogens. In addition, screening and diagnosing wild bird populations are challenging tasks, considering the difficulty in capturing individuals for examination (BRITTINGHAM et al. 1988BRITTINGHAM, M.C.; TEMPLE, S.A.; DUNCAN, R.M. A survey of the prevalence of selected bacteria in wild birds. Journal of Wildlife Diseases, Lawrence, v.24, n.2, p.299-307, 1988. https://doi.org/10.7589/0090-3558-24.2.299
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; LADEAU et al., 2007LADEAU, S.L.; KILPATRICK, A.M.; MARRA, P.P. West Nile virus emergence and large-scale declines of North American bird populations. Nature, London, v.447, n.7145, p.710-713, 2007. https://doi.org/10.1038/nature05829
https://doi.org/10.1038/nature05829...
). Bacteria from the genus Salmonella are among the most important pathogens of interest in human and veterinary medicine due to the zoonotic potential they hold. Hence, this study aimed to review information on Salmonella spp. in free-living birds and their potential in disseminating these pathogens to domestic animals, man, and the environment.

Many species of wild birds coexist with humans and have anthropogenic sources of habitat and nutrition (BRADLEY; ALTIZER, 2007BRADLEY, C.A.; ALTIZER, S. Urbanization and the ecology of wildlife diseases. Trends in Ecology & Evolution, Maryland Heights, v.22, n.2, p.95-102, 2007. https://doi.org/10.1016/j.tree.2006.11.001
https://doi.org/10.1016/j.tree.2006.11.0...
; PALOMO et al., 2013PALOMO, G. et al. Dissemination of Antimicrobial-Resistant Clones of Salmonella enterica Among Domestic Animals, Wild Animals, and Humans. Foodborne Pathogens and Disease, Knoxville, v.10, n.2, p.171-176, 2013. https://doi.org/10.1089/fpd.2012.1288
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). Birds adapted to the urban life are exposed to infection and may act as disseminators of enteric zoonotic pathogens due to several factors, such as intake of contaminated food and water, polluted environments, microclimates with elevated temperature and reduced seasonality, which promote proliferation of vectors and persistence of some parasites, in addition to contact with other stressing agents causing immunosuppression, and aggregation of great number of birds in small areas, which increases the odds of contact with possible hosts (BRADLEY; ALTIZER, 2007BRADLEY, C.A.; ALTIZER, S. Urbanization and the ecology of wildlife diseases. Trends in Ecology & Evolution, Maryland Heights, v.22, n.2, p.95-102, 2007. https://doi.org/10.1016/j.tree.2006.11.001
https://doi.org/10.1016/j.tree.2006.11.0...
; PALOMO et al., 2013PALOMO, G. et al. Dissemination of Antimicrobial-Resistant Clones of Salmonella enterica Among Domestic Animals, Wild Animals, and Humans. Foodborne Pathogens and Disease, Knoxville, v.10, n.2, p.171-176, 2013. https://doi.org/10.1089/fpd.2012.1288
https://doi.org/10.1089/fpd.2012.1288...
). An inadequate habit that contributes to the presence of microorganisms in urbanized environments is bird feeding (JONES; REYNOLDS, 2008JONES, D.N.; REYNOLDS, S.J. Feeding birds in our towns and cities: a global research opportunity. Journal of Avian Biology, Gotemburgo, v.39, n.3, p.265-271, 2008. https://doi.org/10.1111/j.0908-8857.2008.04271.x
https://doi.org/10.1111/j.0908-8857.2008...
), which is related to the increased prevalence of some bacteria in these animals (BRITTINGHAM et al., 1988BRITTINGHAM, M.C.; TEMPLE, S.A.; DUNCAN, R.M. A survey of the prevalence of selected bacteria in wild birds. Journal of Wildlife Diseases, Lawrence, v.24, n.2, p.299-307, 1988. https://doi.org/10.7589/0090-3558-24.2.299
https://doi.org/10.7589/0090-3558-24.2.2...
). This practice may favor emerging diseases due to the stimulation of reproduction in urban environments, resulting in elevated density of birds and increased concentration of feces and stress due to the interactions between individuals (DAOUST; PRESCOTT, 2007DAOUST, P.-Y.; PRESCOTT, J.F. Salmonellosis. In: THOMAS, N.J.; HUNTER, D.B; ATKINSON, C.T. (eds). Infectious Diseases of Wild Birds. Ames: Blackwell, 2007. chap.13, p.270-288. https://doi.org/10.1002/9780470344668.ch13
https://doi.org/10.1002/9780470344668.ch...
).

Some species of birds migrate thousands of kilometers through different continents and carry certain pathogens in this process (HUBÁLEK, 2004HUBÁLEK, Z. An annotated checklist of pathogenic microorganisms associated with migratory birds. Journal of Wildlife Diseases, Lawrence, v.40, n.4, p.639-659, 2004. https://doi.org/10.7589/0090-3558-40.4.639
https://doi.org/10.7589/0090-3558-40.4.6...
; BRUGMAN et al., 2013BRUGMAN, V.A.; HORTON, D.L.; PHIPPS, L.P.; JOHNSON, N.; COOK, A.J.C.; FOOKS, A.R.; BREED, A.C. Epidemiological perspectives on West Nile virus surveillance in wild birds in Great Britain. Epidemiology & Infection, Cambridge, v.141, n.6, p.1134-1142, 2013. https://doi.org/10.1017/S095026881200177X
https://doi.org/10.1017/S095026881200177...
). Approximately 60.3% of all the emerging infectious diseases in humans are zoonoses and 71.8% originated from wild animals (JONES; REYNOLDS, 2008JONES, D.N.; REYNOLDS, S.J. Feeding birds in our towns and cities: a global research opportunity. Journal of Avian Biology, Gotemburgo, v.39, n.3, p.265-271, 2008. https://doi.org/10.1111/j.0908-8857.2008.04271.x
https://doi.org/10.1111/j.0908-8857.2008...
). According to TIZARD (2004)TIZARD, I. Salmonellosis in wild birds. Seminars in Avian and Exotic Pet Medicine, Philadelphia, v.13, n.2, p.50-66, 2004. https://doi.org/10.1053/j.saep.2004.01.008
https://doi.org/10.1053/j.saep.2004.01.0...
, among these infections, salmonellosis is an emerging disease in wild birds and its prevalence have been documented since the 1960s.

Modification of the natural environment by human action may cause a superposition of the natural habitat of birds with urban, agricultural or fishing areas, which may increase the transmission of zoonotic pathogens, such as Salmonella spp. (LILLEHAUG et al., 2005LILLEHAUG, A.; JONASSEN, C.M.; BERGSJØ, B.; HOFSHAGEN, M.; THARALDSEN, J.; NESSE, L.L.; HANDELAND, K. Screening of Feral Pigeon (Colomba livia), Mallard (Anas platyrhynchos) and Graylag Goose (Anser anser) Populations for Campylobacter spp., Salmonella spp., Avian Influenza Virus and Avian Paramyxovirus. Acta Veterinaria Scandinavica, København, v.46, n.4, p.193, 2005. https://doi.org/10.1186/1751-0147-46-193
https://doi.org/10.1186/1751-0147-46-193...
). This bacterium may resist for months in humid soil, feces and water, and may cause new infections in birds (MURRAY, 1991MURRAY, C.J. Salmonellae in the environment. Revue Scientifique et Technique, Paris, v.10, n.3, p.765-785, 1991. https://doi.org/10.20506/rst.10.3.568
https://doi.org/10.20506/rst.10.3.568...
; BÖHM, 1993BÖHM, R. Behavior of selected salmonellae in the environment. Deutsche Tierarztliche Wochenschrift, Berlin, v.100, n.7, p.275-278, 1993. Available from: https://pubmed.ncbi.nlm.nih.gov/8375321/. Access on: 13 Apr. 2018.
https://pubmed.ncbi.nlm.nih.gov/8375321/...
; WINFIELD; GROISMAN, 2003WINFIELD, M.D.; GROISMAN, E.A. Role of Nonhost Environments in the Lifestyles of Salmonella and Escherichia coli. Applied and Environmental Microbiology, Bayreuth, v.69, n.7, p.3687-3694, 2003. https://doi.org/10.1128/AEM.69.7.3687-3694.2003
https://doi.org/10.1128/AEM.69.7.3687-36...
). Its prevalence in free-living birds is influenced by factors such as diet, environment, exposure to antibiotics, infection by pathogenic microorganisms and migration patterns (PALMGREN et al., 1997PALMGREN, H.; SELLIN, M.; BERGSTRÖM, S.; OLSEN, B. Enteropathogenic Bacteria in Migrating Birds Arriving in Sweden. Scandinavian Journal of Infectious Diseases, Umeå, v.29, n.6, p.565-568, 1997. https://doi.org/10.3109/00365549709035895
https://doi.org/10.3109/0036554970903589...
; LU et al., 2003LU, J.; IDRIS, U.; HARMON, B.; HOFACRE, C.; MAURER, J.J.; LEE, M.D. Diversity and succession of the intestinal bacterial community of the maturing broiler chicken. Applied and Environmental Microbiology, Bayreuth, v.69, n.11, p.6816-6824, 2003. https://doi.org/10.1128/AEM.69.11.6816-6824.2003
https://doi.org/10.1128/AEM.69.11.6816-6...
; GABRIEL et al., 2005GABRIEL, I.; MALLET, S.; SIBILLE, P. La microflore digestive des volailles: facteurs de variation et conséquences pour l’animal. INRAE Productions Animales, Saint-Genès-Champanelle, v.18, n.5, p.309-322, 2005. https://doi.org/10.20870/productions-animales.2005.18.5.3535
https://doi.org/10.20870/productions-ani...
; SKOV et al., 2008SKOV, M.N.; MADSEN, J.J.; RAHBEK, C.; LODAL, J.; JESPERSEN, J.B.; JØRGENSEN, J.C.; DIETZ, H.H.; CHRIÉL, M.; BAGGESEN, D.L. Transmission of Salmonella between wildlife and meat-production animals in Denmark. Journal of Applied Microbiology, London, v.105, n.5, p.1558-1568, 2008. https://doi.org/10.1111/j.1365-2672.2008.03914.x
https://doi.org/10.1111/j.1365-2672.2008...
). Salmonellosis in birds occurs as a result of temporary colonization of the digestive tract by environmental strains. In addition, infections caused by strains that are adapted to the host may occur, which may or may not be pathogenic (TIZARD, 2004TIZARD, I. Salmonellosis in wild birds. Seminars in Avian and Exotic Pet Medicine, Philadelphia, v.13, n.2, p.50-66, 2004. https://doi.org/10.1053/j.saep.2004.01.008
https://doi.org/10.1053/j.saep.2004.01.0...
). Hence, depending on the strain, the bird may present an asymptomatic condition or die.

Asymptomatic cases of infection by Salmonella spp. present great relevance. Carriers may shed bacteria without clinical evidence (CONNOLLY et al., 2006CONNOLLY, J.H.; ALLEY, M.R.; DUTTON, G.J.; ROGERS, L.E. Infectivity and persistence of an outbreak strain of Salmonella enterica serotype Typhimurium DT160 for house sparrows (Passer domesticus) in New Zealand. New Zealand Veterinary Journal, Wellington, v.54, n.6, p.329-332, 2006. https://doi.org/10.1080/00480169.2006.36719
https://doi.org/10.1080/00480169.2006.36...
). KLAASSEN et al. (2012)KLAASSEN, M.; HOYE, B.J.; NOLET, B.A.; BUTTEMER, W.A. Ecophysiology of avian migration in the face of current global hazards. Philosophical Transactions of the Royal Society B, London, v.367, n.1596, p.1719-1732, 2012. https://doi.org/10.1098/rstb.2012.0008
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suggest that some stressful conditions may act as a trigger for the bird to develop and disseminate Salmonella in the environment, such as cold weather, behavioral alterations, and the prereproduction cycle (MORENO et al., 2003MORENO, J.; BRIONES, V.; MERINO, S.; BALLESTEROS, C.; SANZ, J.J.; TOMÁS, G. Beneficial effects of cloacal bacteria on growth and fledging size in nestling pied flycatchers (Ficedula hypoleuca) in Spain. The Auk, Oxford, v.120, n.3, p.784-790, 2003. https://doi.org/10.2307/4090108
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).

Some Salmonella strains were identified as specific pathogens of birds in 1889, when Klein isolated Salmonella ser. Gallinarum (BARROW, 1993BARROW, P.A. Salmonella control — past, present and future. Avian Pathology, London, v.22, n.4, p.651-669, 1993. https://doi.org/10.1080/03079459308418954
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) and Rettger identified S. ser. Gallinarum biovar Pullorum in 1899 (RETTGER, 1909RETTGER, L.F. Further studies on fatal septicemia in young chickens, or “white diarrhea”. The Journal of Medical Research, Boston, v.21, n.1, p.115-123, 1909. Available from: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2098883/. Access on: 21 Sep. 2018.
https://www.ncbi.nlm.nih.gov/pmc/article...
). These pathogens cause fowl typhoid and pullorum disease, respectively, which have been more frequently reported in Galliformes reared in domestic environment (GAST, 2008GAST, R.K. Salmonella Infections. In: SAIF, Y.M. (ed). Diseases of Poultry. 12th. Ed. Ames: Blackwell, 2008. chap.16, p.619-665.). In free-living birds, both serotypes were rarely reported. Salmonella ser. Gallinarum biovar Pullorum was isolated from buff-necked ibis (Theristicus caudatus) that lived near a poultry production in Brazil (SOUSA et al., 2010aSOUSA, E.; WERTHER, K.; BERCHIERI JÚNIOR, A. Assessment of Newcastle and infectious bronchitis pathogens, and Salmonella spp. in wild birds captured near poultry facilities. Arquivo Brasileiro de Medicina Veterinária e Zootecnia, Belo Horizonte, v.62, n.1, p.219-223, 2010a. https://doi.org/10.1590/S0102-09352010000100031
https://doi.org/10.1590/S0102-0935201000...
). In the United Kingdom, S. ser. Gallinarum have been isolated from rooks (Corvus frugilegus) and common wood pigeons (Columba palumbus) that lived in regions where fowl typhoid was occurred frequently (HARBOURNE, 1955HARBOURNE, J.F. The Isolation of Salmonella Gallinarum in Wild Birds. Journal of Comparative Pathology and Therapeutics, Amsterdam, v.65, p.250-254, 1955. https://doi.org/10.1016/S0368-1742(55)80023-9
https://doi.org/10.1016/S0368-1742(55)80...
). In 2012, S. ser. Gallinarum was isolated from a red-winged blackbird (Agelaius phoeniceus) in the United States (HAMER et al., 2012HAMER, S.A.; LEHRER, E.; MAGLE, S.B. Wild Birds as Sentinels for Multiple Zoonotic Pathogens Along an Urban to Rural Gradient in Greater Chicago, Illinois. Zoonoses and Public Health, Weinheim, v.59, n.5, p.355-364, 2012. https://doi.org/10.1111/j.1863-2378.2012.01462.x
https://doi.org/10.1111/j.1863-2378.2012...
).

In the scientific literature, a predominance of Salmonella ser. Typhimurium (ST) as a cause of mortality in free-living birds occurs, affecting especially birds from Passeridae and Fringillidae families, which are mostly granivorous species (MIKAELIAN et al., 1997MIKAELIAN, I.; DAIGNAULT, D.; DUVAL, M.C.; MARTINEAU, D. Salmonella infection in wild birds from Quebec. The Canadian Veterinary Journal, Guelph, v.38, n.6, p.385, 1997. Available from: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC1576894/. Access on: 11 Aug. 2018.
https://www.ncbi.nlm.nih.gov/pmc/article...
; HUDSON et al., 2000HUDSON, C.R.; QUIST, C.; LEE, M.D.; KEYES, K.; DODSON, S.V.; MORALES, C.; SANCHEZ, S.; WHITE, D.G.; MAURER, J.J. Genetic Relatedness of Salmonella Isolates from Nondomestic Birds in Southeastern United States. Journal of Clinical Microbiology, Washington, v.38, n.5, p.1860-1865, 2000. https://doi.org/10.1128/JCM.38.5.1860-1865.2000
https://doi.org/10.1128/JCM.38.5.1860-18...
; UNE et al., 2008UNE, Y.; SANBE, A.; SUZUKI, S.; NIWA, T.; KAWAKAMI, K.; KUROSAWA, R.; IZUMIYA, H.; WATANABE, H.; KATO, Y. Salmonella enterica Serotype Typhimurium Infection Causing Mortality in Eurasian Tree Sparrows (Passer montanus) in Hokkaido. Japanese Journal of Infectious Diseases, Shinjuku, v.61, n.2, p.166-167, 2008. Available from: https://www.niid.go.jp/niid/images/JJID/61/166.pdf. Access on: 24 Jun. 2018.
https://www.niid.go.jp/niid/images/JJID/...
; GIOVANNINI et al., 2013GIOVANNINI, S.; PEWSNER, M.; HÜSSY, D.; HÄCHLER, H.; DEGIORGIS, M.-P.R.; VON HIRSCHHEYDT, J.; ORIGGI, F.C. Epidemic of Salmonellosis in Passerine Birds in Switzerland With Spillover to Domestic Cats. Veterinary Pathology, Guelph, v.50, n.4, p.597-606, 2013. https://doi.org/10.1177/0300985812465328
https://doi.org/10.1177/0300985812465328...
; VELARDE et al., 2012VELARDE, R.; PORRERO, M.C.; SERRANO, E.; MARCO, I.; GARCÍA, M.; TÉLLEZ, S.; DOMÍNGUEZ, L.; AYMI, R.; LAVÍN, S. Septicemic salmonellosis caused by Salmonella Hessarek in wintering and migrating Song Thrushes (Turdus philomelos) in Spain. Journal of Wildlife Diseases, Lawrence, v.48, n.1, p.113-121, 2012. https://doi.org/10.7589/0090-3558-48.1.113
https://doi.org/10.7589/0090-3558-48.1.1...
). Epizooties in free-living birds by S. ser. Typhimurium were described for the first time in Switzerland during the 1950s (BOUVIER et al., 1955BOUVIER, G.; BURGISSER, H.; SCHNEIDER, P.A. Observations on diseases in game, birds and fish in 1953 and 1954. Schweizer Archiv für Tierheilkunde, Bern, v.97, p.318-325, 1955.). Since then, several other reports were published. In 1999, an outbreak of gastroenteritis caused by S. ser. Typhimurium DT40 in humans and cats in the center of Sweden was associated with infections and mortality in wild birds, especially in common redpolls (Carduelis flammea) and Eurasian siskins (Carduelis spinus) (TAUNI; ÖSTERLUND, 2000TAUNI, M.A.; ÖSTERLUND, A. Outbreak of Salmonella typhimurium in cats and humans associated with infection in wild birds. Journal of Small Animal Practice, Quedgeley, v.41, n.8, p.339-341, 2000. https://doi.org/10.1111/j.1748-5827.2000.tb03214.x
https://doi.org/10.1111/j.1748-5827.2000...
). Salmonella ser. Typhimurium was pointed as the cause of mortality in wild birds from winter 1997 to summer 1998 in the eastern North America. Most affected species in these areas were pine siskin (Spinus pinus), purple finches (Carpodacus purpureus), evening grosbeaks (Coccothraustes vespertinus) and American goldfinches (Carduelis tristis) (DAOUST et al., 2000DAOUST, P.-Y.; BUSBY, D.G.; FERNS, L.; GOLTZ, J.; MCBURNEY, S.; POPPE, C.; WHITNEY, H. Salmonellosis in songbirds in the Canadian Atlantic provinces during winter-summer 1997-98. The Canadian Veterinary Journal, Guelph, v.41, n.1, p.54-59, 2000. Available from: https://pubmed.ncbi.nlm.nih.gov/10642873/. Access on: 7 Jul. 2017.
https://pubmed.ncbi.nlm.nih.gov/10642873...
). REFSUM et al. (2003)REFSUM, T.; VIKØREN, T.; HANDELAND, K.; KAPPERUD, G.; HOLSTAD, G. Epidemiologic and pathologic aspects of Salmonella Typhimurium infection in passerine birds in Norway. Journal of Wildlife Diseases, Lawrence, v.39, n.1, p.64-72, 2003. https://doi.org/10.7589/0090-3558-39.1.64
https://doi.org/10.7589/0090-3558-39.1.6...
reported an outbreak caused by S. ser. Typhimurium in 64.8% of wild Passeriformes found dead in a bird feeding station, and the following species were most affected: Eurasian siskins (C. spinus), purple finches (C. purpureus), common redpolls (C. flammea) and European greenfinches (Carduelis chloris).

Outbreaks related to free-living birds and humans have also been reported. In Great Britain, the access of sparrows to a kitchen resulted in fecal contamination of food, which originated two outbreaks of gastroenteritis (caused by S. ser. Typhimurium DT40 and DT160) in hospitalized patients (PENFOLD et al., 1979PENFOLD, J.B.; AMERY, H.C.C.; PEET, P.J.M. News and Notes: Gastroenteritis associated with wild birds in a hospital kitchen. British Medical Journal, London, v.2, n.6193, 801-803, 1979. https://doi.org/10.1136/bmj.2.6193.801
https://doi.org/10.1136/bmj.2.6193.801...
). ALLEY et al. (2002)ALLEY, M.R.; CONNOLLY, J.H.; FENWICK, S.G.; MACKERETH, G.F.; LEYLAND, M.J.; ROGERS, L.E.; HAYCOCK, M.; NICOL, C.; REED, C.E.M. An epidemic of salmonellosis caused by Salmonella Typhimurium DT160 in wild birds and humans in New Zealand. New Zealand Veterinary Journal, Wellington, v.50, n.5, p.170-176, 2002. https://doi.org/10.1080/00480169.2002.36306
https://doi.org/10.1080/00480169.2002.36...
reported an outbreak of S. ser. Typhimurium DT160 causing enteric disease in humans and mortality in sparrows (Passer domesticus), European greenfinches (C. chloris), European goldfinches (Carduelis carduelis) and common blackbirds (Turdus merula) that lived in rural areas of New Zealand. More recently, the occurrence of identical genotypes of S. ser. Typhimurium were isolated from wild bird populations and humans in Germany (HAUSER et al., 2009HAUSER, E.; HUEHN, S.; JUNKER, E.; JABER, M.; SCHROETER, A.; HELMUTH, R.; RABSCH, W.; WINTERHOFF, N.; MALORNY, B. Characterisation of a phenotypic monophasic variant belonging to Salmonella enterica subsp. enterica serovar Typhimurium from wild birds and its possible transmission to cats and humans. Berliner und Munchener Tierarztliche Wochenschrift, Berlin, v.122, n.5-6, p.169-177, 2009. Available from: https://europepmc.org/article/med/19517930. Access on: 20 Feb. 2018.
https://europepmc.org/article/med/195179...
).

In addition to the mentioned above, many other serotypes of Salmonella have also been isolated from free-living bird in numerous parts of the world, especially in North America and Europe (Table 1).

Table 1
Occurrence of Salmonella serotypes in wild birds.

A group of birds that deserve special attention are predators, considering that they may identify weakened birds and attack (GRANT et al., 2007GRANT, D.; TODD, P.A.; PENNYCOTT, T. Monitoring wild greenfinch (Carduelis chloris) for Salmonella enterica typhimurium. Ecological Research, Kyoto, v.22, n.4, p.571-574, 2007. https://doi.org/10.1007/s11284-006-0056-2
https://doi.org/10.1007/s11284-006-0056-...
). However, they may harbor Salmonella in greater proportion than nonpredatory birds (RECHE et al., 2003RECHE, M.P.; JIMÉNEZ, P.A.; ALVAREZ, F.; RÍOS, J.E.G.; ROJAS, A.M.; PEDRO, P. Incidence of Salmonellae in Captive and Wild Free-Living Raptorial Birds in Central Spain. Journal of Veterinary Medicine, Series B, Weinheim, v.50, n.1, p.42-44, 2003. https://doi.org/10.1046/j.1439-0450.2003.00623.x
https://doi.org/10.1046/j.1439-0450.2003...
; MILLÁN et al., 2004MILLÁN, J.; ADURIZ, G.; MORENO, B.; JUSTE, R.A.; BARRAL, M. Salmonella isolates from wild birds and mammals in the Basque Country (Spain). Revue Scientifique et Technique, Paris, v.23, n.3, p.905-911, 2004. https://doi.org/10.20506/rst.23.3.1529
https://doi.org/10.20506/rst.23.3.1529...
; MOLINA-LOPEZ et al., 2011MOLINA-LOPEZ, R.A.; VALVERDÚ, N.; MARTIN, M.; MATEU, E.; OBON, E.; CERDÀ-CUÉLLAR, M.; DARWICH, L. Wild raptors as carriers of antimicrobial-resistant Salmonella and Campylobacter strains. Veterinary Record, London, v.168, n.21, p.565, 2011. https://doi.org/10.1136/vr.c7123
https://doi.org/10.1136/vr.c7123...
). A variety of serotypes have been isolated from cloacal swabs or organ samples collected from different species of birds of prey, such as S. ser. Typhimurium, S. ser. Tuindorp, S. ser. Enteritidis, S. ser. Newport and S. ser. Pajala (Table 1). Some species, such as the peregrine falcon (Falco peregrinus), are possible disseminators of these pathogens. HERNANDEZ et al. (2012)HERNANDEZ S.M.; KEEL K.; SANCHEZ S.; TREES E.; GERNER-SMIDT P.; ADAMS J.K.; CHENG Y.; Ray A.; MARTIN G.; PRESOTTO A., RUDES M.G.; BROWN J.; BLEHERT D.S.; COTTRELL W.; MAURER J.J. Epidemiology of a Salmonella enterica subsp. enterica Serovar Typhimurium Strain Associated with a Songbird Outbreak. Applied and Environmental Microbiology, Bayreuth, v.78, n.20, p.7290-7298, 2012. https://doi.org/10.1128/AEM.01408-12
https://doi.org/10.1128/AEM.01408-12...
explain that the diet of this species consists mostly of birds from the Charadridae and Laridae families. Hence, peregrine falcons are migratory birds that reach great distances and may disseminate this pathogen through several areas, including those unoccupied by man.

Migratory birds are epidemiologically relevant for the possibility of acting as long-distance disseminators of pathogens that may affect man and animals (TAUNI; ÖSTERLUND, 2000TAUNI, M.A.; ÖSTERLUND, A. Outbreak of Salmonella typhimurium in cats and humans associated with infection in wild birds. Journal of Small Animal Practice, Quedgeley, v.41, n.8, p.339-341, 2000. https://doi.org/10.1111/j.1748-5827.2000.tb03214.x
https://doi.org/10.1111/j.1748-5827.2000...
). FENLON (1981)FENLON, D.R. Seagulls (Larus spp.) as vectors of salmonellae: an investigation into the range of serotypes and numbers of salmonellae in gull faeces. Epidemiology & Infection, Cambridge, v.86, n.2, p.195-202, 1981. https://doi.org/10.1017/S0022172400068911
https://doi.org/10.1017/S002217240006891...
found that 72% of the serotypes isolated from human cases in Grampian, Scotland, were found in seagulls, and suggested that this was the result of them feeding on untreated sewage disposal. The European herring gull (Larus argentatus) species was reported as a probable source of S. ser. Montivideo for sheep and cattle (COULSON et al., 1983COULSON, J.C.; BUTTERFIELD, J.; THOMAS, C. The herring gull Larus argentatus as a likely transmitting agent of Salmonella montevideo to sheep and cattle. Epidemiology & Infection, Cambridge, v.91, n.3, p.437-443, 1983. https://doi.org/10.1017/S0022172400060472
https://doi.org/10.1017/S002217240006047...
). Other studies reporting Salmonella serotypes in asymptomatic migratory birds were reported in United Kingdom (FRICKER, 1984FRICKER, C.R. A note on salmonella excretion in the black headed gull (Lams ribibundus) feeding at sewage treatment works. Journal of Applied Bacteriology, London, v.56, n.3, p.499-502, 1984. https://doi.org/10.1111/j.1365-2672.1984.tb01380.x
https://doi.org/10.1111/j.1365-2672.1984...
), Czech Republic (LITERÁK et al., 1992LITERÁK, I.; ČÍŽEK, A.; HONZA, M. Examinations of Young Black-headed Gulls (Larus ridibundus) for the Detection of Salmonellae in the Environment. Acta Veterinaria Brno, Brno, v.61, n.2-3, p.141-146, 1992. https://doi.org/10.2754/avb199261020141
https://doi.org/10.2754/avb199261020141...
), Canada (QUESSY; MESSIER, 1992QUESSY, S.; MESSIER, S. Prevalence of Salmonella spp., Campylobacter spp. and Listeria spp. in ring-billed gulls (Larus delawarensis). Journal of Wildlife Diseases, Lawrence, v.28, n.4, p.526-531, 1992. https://doi.org/10.7589/0090-3558-28.4.526
https://doi.org/10.7589/0090-3558-28.4.5...
) Sweden (PALMGREN et al., 2000PALMGREN, H.; MCCAFFERTY, D.; ASPÁN, A.; BROMAN, T.; SELLIN, M.; WOLLIN, R.; BERGSTRÖM, S.; OLSEN, B. Salmonella in sub-Antarctica: low heterogeneity in Salmonella serotypes in South Georgian seals and birds. Epidemiology & Infection, Cambridge, v.125, n.2, p.257-262, 2000. https://doi.org/10.1017/S0950268899004586
https://doi.org/10.1017/S095026889900458...
), Argentina (FRERE et al., 2000FRERE, E.; GANDINI, P.A.; PECK, R.M. Gaviota Cocinera (Larus dominicanus) como vector potencial de patógenos, em la costa patagónica. El Hornero, Buenos Aires, v15, n.02, p.93-97, 2000. Available from: https://ri.conicet.gov.ar/handle/11336/72054. Access on: 10 Jan. 2018.
https://ri.conicet.gov.ar/handle/11336/7...
; LIAKOPOULOS et al., 2016LIAKOPOULOS, A.; OLSEN, B.; GEURTS, Y.; ARTURSSON, K.; BERG, C.; MEVIUS, D.J.; BONNEDAHL, J. Molecular Characterization of Extended-Spectrum Cephalosporin-Resistant Enterobacteriaceae from Wild Birds (Kelp Gulls) in South America. Antimicrobial Agents and Chemotherapy, Washington, v.60, n.11, p.6924-6927, 2016. https://doi.org/10.1128/AAC.01120-16
https://doi.org/10.1128/AAC.01120-16...
), Brazil (ALBARNAZ et al., 2007ALBARNAZ, J.D.; TOSO, J.; CORRÊA, A.A.; SIMÕES C.M.O.; BARARDI, C.R.M. Relationship between the contamination of gulls (Larus dominicanus) and oysters (Crassostrea gigas) with Salmonella serovar Typhimurium by PCR-RFLP. International Journal of Environmental Health Research, Macon, v.17, n.2, p.133-140, 2007. https://doi.org/10.1080/09603120701219816
https://doi.org/10.1080/0960312070121981...
; EBERT et al., 2016EBERT, L.A.; SCHLEMPER, J.C.; PELISSER, M. R; PEREIRA, B. D. A; DA SILVA, M. A; BRANCO, J. O. Pathogenic Bacteria Associated with Kelp Gull Larus dominicanus (Charadriiformes, Laridae) on the Coast of Santa Catarina State-Brazil. International Journal of Current Microbiology and Applied Sciences, Tamilnadu, v.5, n.5, p.458-473, 2016. https://doi.org/10.20546/ijcmas.2016.505.048
https://doi.org/10.20546/ijcmas.2016.505...
) and Chile (LÓPEZ-MARTÍN et al., 2011LÓPEZ-MARTíN, J.; JUNOD, T.; RIQUELME, F.; CONTRERAS, C.; GONZÁLEZ-ACUÑA, D. Detection of Salmonella and Mycobacterium species in seagulls captured in Talcahuano, Chile. Revista Médica de Chile, Santiago, v.139, n.11, p.1496-1502, 2011. https://doi.org/10.4067/S0034-98872011001100017
https://doi.org/10.4067/S0034-9887201100...
).

This study presents published scientific evidence suggesting the direct and indirect role of wild birds in the transmission of Salmonella to humans. Foremost, there are no real evidence for the direct transmission of free-living birds to humans, in addition to the rare cases that occur under exceptional circumstances. Theoretically, several human infections may be transmitted by these animals. However, the scientific base for most of these associations remains speculative. The review demonstrated that carrier birds are probably important in maintaining active sources of infections, which may implicate in epizooties of salmonellosis. However, most of the findings are related to the presence of the pathogen in an asymptomatic manner and the influence of environmental factors in the epidemiology of extensive epizooties remain unknown.

ACKNOWLEDGEMENTS

Not applicable.

  • FUNDING

    This study was financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior – Brasil (CAPES) Finance Code 001.
  • ETHICAL APPROVAL

    Not applicable.
  • AVAILABILITY OF DATA AND MATERIAL

    Data sharing not applicable to this article as no datasets were generated or analyzed during the current study.

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Publication Dates

  • Publication in this collection
    04 Dec 2020
  • Date of issue
    2020

History

  • Received
    06 June 2020
  • Accepted
    20 Sept 2020
Instituto Biológico Av. Conselheiro Rodrigues Alves, 1252 - Vila Mariana - São Paulo - SP, 04014-002 - São Paulo - SP - Brazil
E-mail: arquivos@biologico.sp.gov.br