Frequency of zoonotic bacteria among illegally traded wild birds in Rio de Janeiro

Carlos Alexandre Rey Matias Ingrid Annes Pereira Eliane Moura Falavina dos Reis Dália dos Prazeres Rodrigues Salvatore Siciliano About the authors

Abstract

The illegal wildlife trade may increase the risk of infectious disease transmission, and it may not only cause disease outbreaks in humans but also threaten livestock, native wild populations, and ecosystems' health. Bird species may act as carriers in the transmission of enteric pathogens. However, epidemiological studies on zoonotic bacteria in wild birds are rare in Brazil. From March 2011 to March 2012, we investigated the frequency of Enterobacteriaceae in cloacal swab samples from 109 birds of the passerine and Psittacidae families. These birds were recovered from illegal trade in Rio de Janeiro, Brazil, and sent to a rehabilitation center. Gram-negative bacteria were isolated from 86 wild birds (78.9%). A mean (±SD) of 1.68 (±1.30) different bacterial species were isolated per bird, with a maximum of five bacterial species from three bird species. The most frequently isolated bacteria were Escherichia coli, followed by Enterobacter spp., Klebsiella pneumoniae and other enteric bacteria. Salmonella ser. Typhimurium was isolated from a Temminck's seedeater (Sporophila falcirostris), and two Salmonella ser. Panama were isolated from two specimens of chestnut-capped blackbird (Chrysomus ruficapillus). Of the 70 selected bacterial isolates, 60 exhibited antibiotic resistance. The resistance patterns varied from one to nine of the antibiotics tested. Resistance to ceftiofur was the most prevalent, followed by ampicillin and ceftriaxone. The dissemination potential of resistant strains in situations typically seen in the management of captive birds may become a problem for the conservation of natural bird populations and for public health.

Keywords:
Antibiotic resistance; Enterobacteriaceae; Public health; Salmonella; Wild birds

Introduction

The illegal wildlife trade is considered the most lucrative illegal activity in the world, after weapons and illicit drug commerce.11 Ferreira CM, Glock L. Preliminar diagnosis of the trafficked avifauna in the state of Rio Grande do Sul, Brazil. Biociencias. 2004;12:21-30.

2 Lima R. O tráfico de animais silvestres. In: RENCTAS, ed. Vida silvestre: o estreito limiar entre preservação e destruição - Diagnóstico do tráfico de animais silvestres na Mata Atlântica: Corredores Central e Serra do Mar. Brasília: Dupligráfica; 2007:44–49.

3 Ribeiro LB, Silva MG. O comércio ilegal põe em risco a diversidade das aves no Brasil. Ciênc Cult. 2007;59:4-5.
-44 Alves RRN, Lima JRF, Araujo HFP. The live bird trade in Brazil and its conservation implications: an overview. Bird Conserv Int. 2012;:1-13. According to the Brazilian laws, capturing wild animals and maintaining them in captivity without a legal permit is a crime. Because Brazil is one of the richest countries in the world in terms of biodiversity,55 Mittermeier RA, Fonseca GAB, Rylands AB, Brandon K. A brief history of biodiversity conservation in Brazil. Magadiversity. 2005;1:14-21. birds are captured both for national and international trade. When confiscated by official authorities, these birds are sent to rehabilitation centers.44 Alves RRN, Lima JRF, Araujo HFP. The live bird trade in Brazil and its conservation implications: an overview. Bird Conserv Int. 2012;:1-13.,66 Matias CAR, Oliveira VM, Rodrigues DP, Siciliano S. Summary of the bird species seized in the illegal trade in Rio de Janeiro, Brazil. TRAFFIC Bull. 2012;24:83-86.

After habitat loss, the poaching and hunting of wildlife are considered the most important causes of population declines and could significantly affect an ecosystem's dynamics.77 Redford KH. The empty forest. BioScience. 1992;42:412-422. In addition to these consequences, the risk of disease transmission has to be considered given that captivity allows a more intense contact among species, which favors the transmission of infectious agents.88 Chomel BB, Belotto A, Meslin F. Wildlife, exotic pets, and emerging zoonoses. Emerg Infect Dis. 2007;13:6-11.

9 Alves RRN, Nogueira EEG, Araújo HFP, Brooks SE. Bird-keeping in the Caatinga, NE Brazil. Hum Ecol. 2010;38:147-156.
-1010 Fernandes-Ferreira H, Mendonça SV, Albano C, Ferreira FS, Alves RRN. Hunting, use and conservation of birds in Northeast Brazil. Biodivers Conserv. 2012;21:221-244. Moreover, captive practices enable disease transmission mechanisms that not only can cause outbreaks in humans but also threaten livestock, native wildlife populations, and affect ecosystems' health.1111 Karesh WB, Cook RA, Bennett EL, Newcomb J. Wildlife trade and global disease emergence. Emerg Infect Dis. 2005;11:1000-1002.

Wild birds and migratory species may act as sources of infections in the transmission of different microorganisms and may play a role in the spreading of emerging and re-emerging pathogens.1212 Hubálek Z. An annotated checklist of pathogenic microorganisms associated with migratory birds. J Wildl Dis. 2004;40:639-659.

13 Tsiodras S, Kelesidis T, Kelesidis I, Bauchinger U, Falagas ME. Human infections associated with wild birds. J Infect. 2008;56:83-98.
-1414 Benskin CM, Wilson K, Jones K, Hartley IR. Bacterial pathogens in wild birds: a review of the frequency and effects of infection. Biol Rev Camb Philos Soc. 2009;84:349-373. These birds are susceptible to various bacterial pathogens common to men and domestic animals in addition to other potential pathogenic microorganisms, such as protozoa and viruses.1414 Benskin CM, Wilson K, Jones K, Hartley IR. Bacterial pathogens in wild birds: a review of the frequency and effects of infection. Biol Rev Camb Philos Soc. 2009;84:349-373.,1515 Kruse H, Kirkemo A, Handeland K. Wildlife as source of zoonotic infections. Emerg Infect Dis. 2004;10:2067-2072.

Studies on the microbiota of wild birds are rare or limited to a small number of animals, and those addressing the prevalence of Enterobacteriaceae are especially focused on certain groups, such as seagulls. More specifically, research on passerines covered outbreaks with high mortality, which provides no information on the prevalence of pathogens in apparently healthy animals. Thus, the role of these birds as reservoirs of bacterial pathogens may indeed be underestimated.1414 Benskin CM, Wilson K, Jones K, Hartley IR. Bacterial pathogens in wild birds: a review of the frequency and effects of infection. Biol Rev Camb Philos Soc. 2009;84:349-373.

Zoonotic gram-negative bacteria previously isolated from both apparently healthy and sick avian hosts included Salmonella spp., Escherichia coli, Campylobacter spp., Yersinia spp., Klebsiella spp. and Enterobacter spp. Except for the last two etiologic agents, which do not cause disease under normal conditions, these bacteria are responsible for gastroenteritis, respiratory symptoms, septicemia, and even mortality in humans.1414 Benskin CM, Wilson K, Jones K, Hartley IR. Bacterial pathogens in wild birds: a review of the frequency and effects of infection. Biol Rev Camb Philos Soc. 2009;84:349-373.

15 Kruse H, Kirkemo A, Handeland K. Wildlife as source of zoonotic infections. Emerg Infect Dis. 2004;10:2067-2072.
-1616 Steele CM, Brown RN, Botzler RG. Prevalences of zoonotic bacteria among seabirds in rehabilitation centers along the pacific coast of California and Washington, USA. J Wildl Dis. 2005;41:235-244.

The use of antibiotics in animals to control bacterial infections or as growth promoters in poultry production may result in the selection of resistant strains of pathogenic bacteria as much as those that form the normal microbiota. These practices are considered the main factor for triggering the emergence, selection and spread of resistant microorganisms, both in veterinary and human medicine. Although species do not have contact with antibiotics in the wild, they can be infected by wild birds that act as carriers given that antibiotic-resistant bacteria have been isolated in these animals. In addition to the potential problem for wildlife conservation, the spread of multi-drug resistant strains may have implications for public health. The manipulation of these animals and the disposal of their waste represent a hazard for the professionals involved in the surveillance/policing activities, such as veterinarians, biologists, and caregivers.1414 Benskin CM, Wilson K, Jones K, Hartley IR. Bacterial pathogens in wild birds: a review of the frequency and effects of infection. Biol Rev Camb Philos Soc. 2009;84:349-373.

15 Kruse H, Kirkemo A, Handeland K. Wildlife as source of zoonotic infections. Emerg Infect Dis. 2004;10:2067-2072.
-1616 Steele CM, Brown RN, Botzler RG. Prevalences of zoonotic bacteria among seabirds in rehabilitation centers along the pacific coast of California and Washington, USA. J Wildl Dis. 2005;41:235-244.

To better assess the risk of exposure to zoonotic bacteria carried by wild birds for these professionals, we conducted a prevalence survey in a rehabilitation center to describe and compare the frequency of Enterobacteriaceae among groups of birds. The potential pathogenicity to humans was analyzed by the presence of toxin genes in selected isolates of E. coli. Furthermore, we tested the antibiotic resistance in selected strains that were representative of the isolated bacterial species.

Materials and methods

Wild bird specimens where sampled upon arrival at the Rehabilitation Center of Wild Animals (CETAS) in Seropédica, Rio de Janeiro State, Brazil, after being confiscated from local illegal trade markets by the authorities from March 2011 to March 2012. The scientific nomenclature of the bird species follows the Brazilian Ornithological Records Committee (CBRO). Cloacal samples were obtained from one hundred and nine birds of 30 species that were randomly chosen in a total of nine apprehensions. The samples were taken following clinical procedures. Swabs were introduced in Cary Blair medium under refrigerated conditions and sent to the Enterobacteria Laboratory of the Oswaldo Cruz Institute (FIOCRUZ), in Rio de Janeiro, Brazil for microbiological assays. All the procedures were approved by the Chico Mendes Institute of Biodiversity Conservation (SISBIO no 26383-2) and by the Fiocruz Ethics Committee on the Use of Animals (LW - 1/13).

The collected material was transferred to a nutrient broth (Difco™; 37 °C/18-24 h). Then, the samples were enriched in a Rappaport-Vassiliadis broth (42 °C overnight), a Silliker medium and a Muller-Kauffmann medium (37 °C/18-24 h). Next, the cultures were plated for isolation on Hektoen enteric agar (Oxoid™; 37 °C/18-24 h). Representatives of all the distinct colonies were confirmed in a triple sugar iron test (Difco™) and inoculated into a SIM medium for the biochemical characterization of several parameters such as the susceptibility to l-lysine decarboxylase, citrate as a carbon source, mobility, hydrogen sulfide production, glucose and lactose fermentation as well as the indole production. The presumptive diagnosis of the distinct gram-negative isolates was performed by the biochemical tests recommended by Murray et al.1717 Murray PR, Baron EJ, Pfaller MA, Tenover FC, Yolken RH, eds. Manual of Clinical Microbiology. 6th ed. Washington, DC: ASM Press; 1995. and Murray et al.1818 Murray PR, Baron EJ, Jorgensen JH, Landry ML, Pfaller MA, eds. Manual of Clinical Microbiology. 9th ed. Washington, DC: ASM Press; 2007..

The subspecies of Salmonella spp. were determined using substrates according to Grimont and Weill.1919 Grimont PAD, Weill FX. Antigenic Formulae of the Salmonella Serovars. 9th ed. WHO Collaborating Centre for Reference and Research on Salmonella; 2007. The antigenic characterization, which included an induction/absorption phase to recognize the somatic and flagellar fraction, was performed by slide agglutination with somatic and flagellar poly- and monovalent antigens based on the Kaufmann-White scheme.

To compare the frequencies of bacteria isolated from groups of birds, Fisher's exact test was performed using the SPSS software package. A two-way general linear model analysis of variance (ANOVA) was used to examine the differences in species richness of bacteria isolated from different bird families and from the most common bird species. p values of 0.05 or less were considered significant. Species richness values were square-root transformed for normality.

A susceptibility test was performed with 70 isolates of E. coli, Klebsiella spp. and Salmonella spp., from 54 birds using the minimum inhibitory concentration assay (MIC) in agar and broth to determine the lowest concentrations of different antimicrobial drugs. Each one was evaluated in a serial dilution according to the protocol described by the Clinical and Laboratory Standards Institute (CLSI)2020 CLSI (Clinical and Laboratory Standards Institute). Performance Standards for Antimicrobial Susceptibility: Twenty-second Information Supplement - Document M100-S23. Wayne, PA: Clinical and Laboratory Standards Institute;2013. with ampicillin, ceftriaxone, ceftiofur, tetracycline, sulfamethoxazole/trimethoprim 19:1, chloramphenicol, gentamicin, nalidixic acid, ciprofloxacin, enrofloxacin, and nitrofurantoin. The following reference strains were used for the quality control of the antimicrobial susceptibility test: Staphylococcus aureus ATCC25923, Pseudomonas aeruginosa ATCC27853, Enterococcus faecalis ATCC29212 and E. coli ATCC25922.

E. coli strains were selected to identify the presence of toxin genes with the multiplex PCR protocols established by Almeida et al.2121 Almeida PM, Arais LR, Andrade JR, Prado EH, Irino K, Cerqueira AM. Characterization of atypical enteropathogenic Escherichia coli (aEPEC) isolated from dogs. Vet Microbiol. 2012;158:420-424. used for the primary screening of enteropathogens in the Enterobacteria Laboratory of the Oswaldo Cruz Institute (FIOCRUZ), Rio de Janeiro, Brazil. The following genes were investigated: eaeA, stx1, stx2, LT, ST, eagg and ipaH.

Results

The most common sampled bird species were passerines that belonged to the families Emberizidae and Thraupidae (Table 1). Gram-negative bacteria were isolated from 86 of the 109 wild birds sampled (78.9%). A mean (±SD) of 1.68 (±1.30) different bacterial species were isolated per bird, with a maximum of five bacteria from three distinct bird species: a rufous-collared Sparrow (Zonotrichia capensis), a tsayaca Tanager (Tangara sayaca), and a green-winged saltator (Saltator similis). The most frequent isolated bacteria were E. coli, which were prevalent in 55 animals. The next most often isolated bacteria were, in decreasing order, Enterobacter spp. and Klebsiella pneumoniae (Table 2). Salmonella ser. Typhimurium was isolated from a Temminck's seedeater (Sporophila falcirostris), and two Salmonella ser. Panama were isolated from two specimens of chestnut-capped blackbird (Chrysomus ruficapillus) that were kept together in the same cage.

Table 1
Wild birds sampled in the CETAS, Rio de Janeiro (Brazil) from March 2011 to March 2012. The total number of individual bird samples are shown.
Table 2
Enterobacteriaceae from cloacal samples of wild birds in the CETAS, Rio de Janeiro, Brazil. The samples were collected from March 2011 to March 2012. The frequency of Enterobacteriaceae isolated from each bird family sampled are shown.

There were no significant differences in the frequencies of microorganism among the most common bird species, i.e., saffron finch (n = 15), blue-black grassquit (n = 11), and double-collared seedeater (n = 11), according to Fisher's exact test (p < 0.05). Likewise, based on Fisher's exact test (p < 0.05), species of Enterobacteriaceae were significantly more frequent in birds of the families Thraupidae (100%; n = 16), Cardinalidae (100%; n = 8), Turdidae (100%; n = 6), and Psittacidae (100%; n = 3) compared to birds of the families Icteridae (91.7%; n = 12) and Emberizidae (63.3%; n = 60; p = 0.003). The E. coli occurrence was significantly higher in birds of the family Psittacidae (100%; n = 3) than in birds of the families Thraupidae (87.5%; n = 16), Turdidae (83.3%; n = 6), Cardinalidae (62.5%; n = 8), Icteridae (58.3%; n = 12), and Emberizidae (28.3%; n = 60; p < 0.05). The frequency of K. pneumoniae was significantly higher in birds of the family Turdidae (66.7%; n = 6) compared to birds of the families Thraupidae (56.3%; n = 16), Icteridae (50%; n = 12), Cardinalidae (50%; n = 8), and Emberizidae (21.7%; n = 60: p = 0.01).

The Enterobacteriaceae mean (±SD) species richness for each family was 1.1 (±1.06) in Emberizidae, 2.62 (±1.08) in Thraupidae, 2.16 (±1.46) in Icteridae, 2.62 (±1.40) in Cardinalidae, 2.33 (±1.03) in Turdidae, and 1.33 (±0.57) in Psittacidae. These differences were significant (F = 6.71, p < 0.05) based on a general linear model ANOVA (Tukey's post hoc test: Thraupidae > Emberizidae, p < 0.05; Cardinalidae > Emberizidae, p = 0.01). The mean bacterial species richness for the most common wild bird species was 1.26 (±0.96) for saffron finch, 0.81 (±0.98) for blue-black grassquit, and 0.81 (±0.75) for double-collared seedeater. These differences were not significant (DF = 1.08, p = 0.35) based on a general linear model ANOVA.

The eaeA gene was present in five of 61 E. coli isolates obtained from a white-necked thrush (Turdus albicollis), a chestnut-bellied seed-finch (Sporophila angolensis), a sayaca tanager (T. sayaca), a chestnut-capped blackbird (C. ruficapillus), and a chopi blackbird (Gnorimopsar chopi). The stx2 gene was simultaneously present in the chopi blackbird sample.

Antibiotic resistance was present in 60 of the 70 selected bacterial isolates (Table 3). The resistance patterns varied from one to nine of the antibiotics tested. The resistance to ceftiofur (71.67%) was the most frequent, followed by ampicillin (46.67%) and ceftriaxone (35%).

Table 3
Enterobacteriaceae isolated from wild birds in the CETAS, Rio de Janeiro, Brazil, from March 2011 to March 2012. These bacteria were tested for antibiotic resistance.

Discussion

E. coli was the most frequently isolated bacteria from wild birds in this study, and its frequency was significantly higher in Psittacidae birds than in passerines. This microorganism is the most abundant facultative bacterial species in the normal microbiota of the large intestines of animals and humans,2222 Gopee NV, Adesiyun AA, Caesar K. A longitudinal study of Escherichia coli strains isolated from captive mammals, birds and reptiles in Trinidad. J Zoo Wildl Med. 2000;31:353-360. and it has been isolated from a range of bird species, such as passerines.1414 Benskin CM, Wilson K, Jones K, Hartley IR. Bacterial pathogens in wild birds: a review of the frequency and effects of infection. Biol Rev Camb Philos Soc. 2009;84:349-373. However, its prevalence is higher in carnivorous or omnivorous bird species than in granivorous birds, such as most passerines in our study, which have a lower prevalence of this pathogen.1616 Steele CM, Brown RN, Botzler RG. Prevalences of zoonotic bacteria among seabirds in rehabilitation centers along the pacific coast of California and Washington, USA. J Wildl Dis. 2005;41:235-244. The higher frequency of E. coli in our study could be explained in light of the poor sanitary conditions under which the animals were maintained after being captured in the wild.

Enteropathogenic strains have been isolated from healthy or diseased wild birds, which may be carriers of E. coli strains resistant to antibiotics.1212 Hubálek Z. An annotated checklist of pathogenic microorganisms associated with migratory birds. J Wildl Dis. 2004;40:639-659. Of the five E. coli isolates that carried the eaeA gene, one carried simultaneously the stx2 gene. The presence of both genes classifies the strain as an enteropathogenic (EPEC) or enterohemorrhagic (EHEC) E. coli.

The low frequency of Salmonella spp. isolated in this study is in agreement with previous studies with apparently healthy wild birds.2323 Tizard I. Salmonellosis in wild birds. Semin Avian Exot Pet Med. 2004;13:50-66.,2424 Abulreesh HH, Goulder R, Scott GW. Wild birds and human pathogens in the context of ringing and migration. Ringing Migr. 2007;23:193-200. In spite of the low detection rate in the sampled animals and of the difficulty to collect biological material from birds seized in illegal wildlife trade, our results indicate that the isolated serovars circulate in natural bird populations. Several studies revealed that Salmonella ser. Typhimurium and Salmonella ser. Panama circulate in Brazil and in other countries and can be isolated from human and animal biological sources.2525 Bessa MC, Costa M, Cardoso M. Prevalence of Salmonella sp. carrier pigs in slaghterhouses of Rio Grande do Sul, Brazil. Pesq Vet Bras. 2004;24:80-84.

26 Loureiro ECB, Marques NDB, Ramos FLP, Reis EMF, Rodrigues DP, Hofer E. Salmonella serovars of human origin identified in Pará State, Brazil from 1991 to 2008. Rev Pan-Amaz Saúde. 2010;1:93-100.
-2727 Kich JD, Coldebella A, Morés N, et al. Prevalence, distribution, and molecular characterization of Salmonella recovered from swine finishing herds and a slaughter facility in Santa Catarina, Brazil. Int J Food Microbiol. 2011;151:307-313.

Salmonella ser. Typhimurium is frequently associated with disease in several mammalian and avian host species, and it was shown to be common in outbreaks that affected humans and livestock, especially poultry, until the 1990s.2828 Hofer E, Filho SJS, Reis EMF. Prevalence of Salmonella serovars isolated from birds in Brazil. Pesq Vet Bras. 1997;17:55-62.,2929 Rabsch W, Andrews HL, Kingsley RA, et al. Salmonella enterica serotype Typhimurium and its host-adapted variants. Infect Immun. 2002;70:2249-2255. Outbreaks of Salmonella ser. Typhimurium infections in humans that had contact with wild passerine birds have been described in several European countries as well as in the U.S.A. and New Zealand.3030 Kapperud G, Stenwig H, Lassen J. Epidemiology of Salmonella typhimurium O:4-12 infection in Norway. Am J Epidemiol. 1998;147:774-782.

31 Refsum T, Vikoren T, Handeland K, Kapperud G, Holstad G. Epidemiologic and pathologic aspects of Salmonella typhimurium infection in passerine birds in Norway. J Wildl Dis. 2003;39:64-72.
-3232 Thornley CN, Simmons GC, Callaghan ML, et al. First incursion of Salmonella enterica serotype Typhimurium DT160 into New Zealand. Emerg Infect Dis. 2003;9:493-495. Instead, serovar Panama is not frequently isolated in epizooties and human outbreaks in Brazil.2828 Hofer E, Filho SJS, Reis EMF. Prevalence of Salmonella serovars isolated from birds in Brazil. Pesq Vet Bras. 1997;17:55-62.

Several of the isolated bacteria, such as K. pneumoniae, Enterobacter spp., Proteus spp., Providencia spp. and Morganella morganii, are known or suspected to cause diseases in humans and are often associated with nosocomial infections.1616 Steele CM, Brown RN, Botzler RG. Prevalences of zoonotic bacteria among seabirds in rehabilitation centers along the pacific coast of California and Washington, USA. J Wildl Dis. 2005;41:235-244.

Antibiotic resistance in gram-negative bacteria has been reported in other studies of wild birds.1616 Steele CM, Brown RN, Botzler RG. Prevalences of zoonotic bacteria among seabirds in rehabilitation centers along the pacific coast of California and Washington, USA. J Wildl Dis. 2005;41:235-244.,3333 Tsubokura M, Matsumoto A, Otsuki K, Animas SB, Sanekata T. Drug resistance and conjugative R plasmids in Escherichia coli strains isolated from migratory waterfowl. J Wildl Dis. 1995;31:352-357.

34 Nascimento AMA, Cursino L, Gonçalves-Dornelas H, Reis A, Chartone-Souza E, Marini MA. Antibiotic-resistant gram-negative bacteria in birds from the Brazilian Atlantic Forest. The Condor. 2003;105:358-361.

35 Hasan B, Sandegren L, Melhus A, et al. Antimicrobial drug-resistant Escherichia coli in wild birds and free-range poultry, Bangladesh. Emerg Infect Dis. 2012;18:2055-2058.

36 Carroll D, Wang J, Fanning S, McMahon BJ. Antimicrobial resistance in wildlife: implications for public health. Zoon Public Health. 2015;62:534-542.
-3737 Greig J, Rajic A, Young I, Mascarenhas M, Waddell L, LeJeune J. A scoping review of the role of wildlife in the transmission of bacterial pathogens and antimicrobial resistance to the food chain. Zoon Public Health. 2015;62:269-284. Resistance to ampicillin is consistent with the results obtained by Steele et al.1616 Steele CM, Brown RN, Botzler RG. Prevalences of zoonotic bacteria among seabirds in rehabilitation centers along the pacific coast of California and Washington, USA. J Wildl Dis. 2005;41:235-244., Tsubokura et al.3333 Tsubokura M, Matsumoto A, Otsuki K, Animas SB, Sanekata T. Drug resistance and conjugative R plasmids in Escherichia coli strains isolated from migratory waterfowl. J Wildl Dis. 1995;31:352-357., Nascimento et al.3434 Nascimento AMA, Cursino L, Gonçalves-Dornelas H, Reis A, Chartone-Souza E, Marini MA. Antibiotic-resistant gram-negative bacteria in birds from the Brazilian Atlantic Forest. The Condor. 2003;105:358-361., Silva-Hidalgo et al.3838 Silva-Hidalgo G, López-Valenzuela M, Juárez-Barranco F, Montiel-Vázquez E, Valenzuela-Sánchez B. Salmonella serovars and antimicrobial resistance in strains isolated from wild animals in captivity in Sinaloa, Mexico. Jpn J Vet Res. 2014;62:129-134., and Carroll et al.3737 Greig J, Rajic A, Young I, Mascarenhas M, Waddell L, LeJeune J. A scoping review of the role of wildlife in the transmission of bacterial pathogens and antimicrobial resistance to the food chain. Zoon Public Health. 2015;62:269-284. The same is valid for the resistance to ceftiofur, as reported by Steele et al.1616 Steele CM, Brown RN, Botzler RG. Prevalences of zoonotic bacteria among seabirds in rehabilitation centers along the pacific coast of California and Washington, USA. J Wildl Dis. 2005;41:235-244.. Likewise, it is important to note the number of multi-drug resistant E. coli and K. pneumoniae strains, both of which are important nosocomial pathogens.1616 Steele CM, Brown RN, Botzler RG. Prevalences of zoonotic bacteria among seabirds in rehabilitation centers along the pacific coast of California and Washington, USA. J Wildl Dis. 2005;41:235-244.

These resistance profiles stress the importance of a surveillance program to prevent the impact of these pathogenic microorganisms on public health.3939 Berendonk TU, Manaia CM, Merlin M, et al. Tackling antibiotic resistance: the environmental framework. Nat Rev Microbiol. 2015;13:310-317. A considerable number of isolates and the three Salmonella strains were resistant to ceftiofur and ceftriaxone, which are third generation cephalosporins. Ceftiofur is used in veterinary medicine, while ceftriaxone is prescribed in the treatment of severe human Salmonella infections.

The presence of antibiotic resistance in wildlife may be a proof of the impact of human activities on natural ecosystems.4040 Blanco G, Lemus JA, Grande J, et al. Geographical variation in cloacal microflora and bacterial antibiotic resistance in a threatened avian scavenger in relation to diet and livestock farming practices. Environ Microbiol. 2007;9:1738-1749. Wild birds may acquire and disseminate enteric bacteria, including resistant strains, by the fecal-oral route through species that act as carriers, such as insects, rodents and other birds, apart from the contact with human waste and contaminated food. In these cases, they act as reservoirs, carriers or sentinels of resistant bacterial pathogens.1616 Steele CM, Brown RN, Botzler RG. Prevalences of zoonotic bacteria among seabirds in rehabilitation centers along the pacific coast of California and Washington, USA. J Wildl Dis. 2005;41:235-244.,3636 Carroll D, Wang J, Fanning S, McMahon BJ. Antimicrobial resistance in wildlife: implications for public health. Zoon Public Health. 2015;62:534-542.,4141 Hilbert F, Smulders FJM, Chopra-Dewasthaly R, Paulsen P. Salmonella in the wildlife-human interface. Food Res Int. 2012;45:603-608.,4242 Wellington EMH, Boxall ABA, Cross P, et al. The role of the natural environment in the emergence of antibiotic resistance in Gram-negative bacteria. Lancet Infect Dis. 2013;13:155-165.

Multiresistant phenotypes in wild bird feces represent an important evidence of the transmission of pathogens and of antimicrobial resistance mechanisms, both domestically and across international borders, that are fostered by the trade of wild animals and a close contact with humans. Additional studies in natural environments, which should include the microbiological monitoring of professionals that directly manage wild animals, are essential to better understand the source of resistant strains isolated from wildlife.

References

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    Ferreira CM, Glock L. Preliminar diagnosis of the trafficked avifauna in the state of Rio Grande do Sul, Brazil. Biociencias 2004;12:21-30.
  • 2
    Lima R. O tráfico de animais silvestres. In: RENCTAS, ed. Vida silvestre: o estreito limiar entre preservação e destruição - Diagnóstico do tráfico de animais silvestres na Mata Atlântica: Corredores Central e Serra do Mar Brasília: Dupligráfica; 2007:44–49.
  • 3
    Ribeiro LB, Silva MG. O comércio ilegal põe em risco a diversidade das aves no Brasil. Ciênc Cult 2007;59:4-5.
  • 4
    Alves RRN, Lima JRF, Araujo HFP. The live bird trade in Brazil and its conservation implications: an overview. Bird Conserv Int 2012;:1-13.
  • 5
    Mittermeier RA, Fonseca GAB, Rylands AB, Brandon K. A brief history of biodiversity conservation in Brazil. Magadiversity 2005;1:14-21.
  • 6
    Matias CAR, Oliveira VM, Rodrigues DP, Siciliano S. Summary of the bird species seized in the illegal trade in Rio de Janeiro, Brazil. TRAFFIC Bull 2012;24:83-86.
  • 7
    Redford KH. The empty forest. BioScience 1992;42:412-422.
  • 8
    Chomel BB, Belotto A, Meslin F. Wildlife, exotic pets, and emerging zoonoses. Emerg Infect Dis 2007;13:6-11.
  • 9
    Alves RRN, Nogueira EEG, Araújo HFP, Brooks SE. Bird-keeping in the Caatinga, NE Brazil. Hum Ecol 2010;38:147-156.
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    Fernandes-Ferreira H, Mendonça SV, Albano C, Ferreira FS, Alves RRN. Hunting, use and conservation of birds in Northeast Brazil. Biodivers Conserv 2012;21:221-244.
  • 11
    Karesh WB, Cook RA, Bennett EL, Newcomb J. Wildlife trade and global disease emergence. Emerg Infect Dis 2005;11:1000-1002.
  • 12
    Hubálek Z. An annotated checklist of pathogenic microorganisms associated with migratory birds. J Wildl Dis 2004;40:639-659.
  • 13
    Tsiodras S, Kelesidis T, Kelesidis I, Bauchinger U, Falagas ME. Human infections associated with wild birds. J Infect 2008;56:83-98.
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    Benskin CM, Wilson K, Jones K, Hartley IR. Bacterial pathogens in wild birds: a review of the frequency and effects of infection. Biol Rev Camb Philos Soc 2009;84:349-373.
  • 15
    Kruse H, Kirkemo A, Handeland K. Wildlife as source of zoonotic infections. Emerg Infect Dis 2004;10:2067-2072.
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    Steele CM, Brown RN, Botzler RG. Prevalences of zoonotic bacteria among seabirds in rehabilitation centers along the pacific coast of California and Washington, USA. J Wildl Dis 2005;41:235-244.
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    Murray PR, Baron EJ, Pfaller MA, Tenover FC, Yolken RH, eds. Manual of Clinical Microbiology 6th ed. Washington, DC: ASM Press; 1995.
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Publication Dates

  • Publication in this collection
    Oct-Dec 2016

History

  • Received
    30 Apr 2015
  • Accepted
    6 Mar 2016
Sociedade Brasileira de Microbiologia USP - ICB III - Dep. de Microbiologia, Sociedade Brasileira de Microbiologia, Av. Prof. Lineu Prestes, 2415, Cidade Universitária, 05508-900 São Paulo, SP - Brasil, Ramal USP 7979, Tel. / Fax: (55 11) 3813-9647 ou 3037-7095 - São Paulo - SP - Brazil
E-mail: bjm@sbmicrobiologia.org.br