Open Access

Campylobacter coli infection in pet birds in southern Italy

  • Ludovico Dipineto1Email author,
  • Luca Borrelli1,
  • Antonino Pace1,
  • Violante Romano1,
  • Stefano D’Orazio1,
  • Lorena Varriale1,
  • Tamara Pasqualina Russo1 and
  • Alessandro Fioretti1
Acta Veterinaria Scandinavica201759:6

https://doi.org/10.1186/s13028-016-0271-y

Received: 30 July 2016

Accepted: 20 December 2016

Published: 6 January 2017

Abstract

Avian species are considered as the main reservoir of Campylobacter spp. However, few data are available on the presence of this microorganism in pet birds. This study was therefore performed to determine the prevalence of Campylobacter spp. in pet birds bred in southern Italy. Faecal samples were collected from 88 cages housing different species of pet birds and examined by bacteriological culture and polymerase chain reaction. A total of 13.6% of the cage samples were positive for Campylobacter coli. Other Campylobacter spp. were not found. The study shows that C. coli can be isolated from the cages of apparently healthy pet birds, which should therefore be considered as potential carriers of C. coli and a possible source of infection for humans and companion animals.

Keywords

Campylobacter spp. Campylobacter coli Avian speciesPet birdsZoonosis

Findings

Thermotolerant Campylobacter spp., mainly Campylobacter jejuni and Campylobacter coli, are the most commonly reported bacteria in enteric infections in humans. The incidence of human campylobacteriosis has increased in both developed and developing countries over the last 10 years [1]. These bacterial species colonize the intestinal mucosa of most warm-blooded animals, including food-producing animal species and humans [2].

Several avian species are considered the main reservoirs of Campylobacter spp. [3, 4]. Nevertheless, current scientific knowledge on the presence of Campylobacter spp. in pet birds is scarce. To address this lack of information, the present study was undertaken to assess the presence of Campylobacter spp. in pet birds bred in southern Italy.

The study was carried out from July to December 2015 in 14 privately owned bird farms located in the Campania region, southern Italy. Sampling was conducted with the approval of the owners. In each farm, the bird population ranged from 20 to 100 birds. Pooled faecal samples were obtained from the floor of 88 cages with birds belonging to the families of Estrildidae (33 cages with 118 birds), Fringillidae (28 cages with 64 birds) and Psittacidae (27 cages with 43 birds) (Table 1). The cage was used as an epidemiological unit, and each cage housed from one to five birds. All birds were apparently in healthy condition and none received any antimicrobial treatment during the study period.
Table 1

Family and species of birds examined, related bird populations and number of cages tested with percentage of cages being positive for Campylobacter coli

Family

Birds tested

Bird population/number of cages tested

Number of positive/pooled fecal samples tested (%)

Estrildidae

Erythrura gouldiae

67/22

0/22 (0%)

Lonchura striata domestica

16/4

0/4 (0%)

Taeniopygia guttata

35/7

7/7 (100%)

Fringillidae

Carduelis carduelis

18/9

0/9 (0%)

Serinus canaria

46/19

0/19 (0%)

Psittacidae

Agapornis spp.

20/10

2/10 (20%)

Amazona spp.

6/6

3/6 (50%)

Arinae subfamily

6/3

0/3 (0%)

Cacatuidae family

2/2

0/2 (0%)

Loriinae subfamily

2/1

0/1 (0%)

Melopsittacus undulatus

2/1

0/1 (0%)

Nymphicus hollandicus

2/1

0/1 (0%)

Psittacus erithacus

3/3

0/3 (0%)

Total

 

225/88

12/88 (13.6%)

Bird population refers to the total number of birds housed in the total number of cages examined

Before the collection of faecal samples, a sheet of sterile aluminum foil was placed under the grid of each cage overnight. Faecal samples were then collected by sterile cotton tipped swabs. Each sample swab was stored in Amies Charcoal Transport Medium (Oxoid, Basingstoke, UK) at 4 °C, transported to the laboratory, and analyzed within 2 h of collection. Samples were inoculated into Bolton selective enrichment broth (Oxoid) and incubated at 42 °C for 48 h under microaerobic conditions provided by CampyGen (Oxoid). Subsequently, each sample was streaked onto Campylobacter blood-free selective agar (modified charcoal cefoperazone deoxycholate agar; Oxoid) with the corresponding supplement (SE 155; Oxoid). The plates were examined for typical Campylobacter colonies after additional incubation at 42 °C for 48 h under microaerobic conditions. The suspected colonies were purified on sheep blood agar (Oxoid) and finally incubated for 24 h at 42 °C. Colonies comprising curved or spiral motile rods were examined by phase contrast microscopy, presumptively identified as Campylobacter spp. and submitted to a multiplex polymerase chain reaction (PCR) analysis following the procedures described by Gargiulo et al. [5].

All positive isolates were tested for the antimicrobial susceptibility by using the disk diffusion method and breakpoints as suggested by Sifré et al. [6]. Because few breakpoints are available for Campylobacter spp., only ciprofloxacin (5 μg), erythromycin (15 μg), and tetracycline (30 μg) were tested.

Twelve out of the 88 cages [13.6%; 95% confidence interval (CI) 7.6–23.0%] were positive for a Campylobacter spp., which in all cases was identified as C. coli. Seven out of 33 cages with bids of the Estrildidae family (21.2%; 95% CI 9.6–39.4%) and five out of 27 cages with birds of the Psittacidae family (18.5%; 95% CI 7.0–38.8%) were infected with C. coli, while all cages (n = 28) with birds of the Fringillidae family were negative (Table 1). Out of the 14 farms, five farms had infected birds (35.7%; 95% CI 14.0–64.4%). All C. coli isolates were sensitive to erythromycin and resistant to tetracycline and ciprofloxacin.

Except for a study reporting a prevalence of campylobacteriosis in pet birds in Argentina to 19.0% [7], data on the occurrence of campylobacteriosis in pet birds are scarce. In our study, 13.6% of the cage samples were found positive for C. coli. The majority of the positive samples (7/12) originated from Taeniopygia guttata species in which C. coli was found in all samples (7/7 species samples) followed by Amazona spp. (3/12 positive samples; 3/6 species samples) and Agapornis spp. (2/12 positive samples; 2/10 species samples).

This study shows that C. coli may be excreted in the faeces of apparently healthy pet birds. Pet birds may be a potential source of C. coli transmission to humans and the risk of transmission of antimicrobial resistant bacteria between pet birds and other animal species and humans should be considered. The adoption of good hygiene practices when handling pet birds should be promoted.

Declarations

Authors’ contributions

LD and LB planned the study. LB, VR, SD and AP collected the samples. AP, TPR and LV performed the laboratory analyses. LD and AF obtained the funding and coordinated the study. LD, VR and SD drafted the manuscript. All authors read and approved the final manuscript.

Acknowledgements

The authors would like to thank the Campania region, which financially supported this project (Legge 5/2002 ann.tà 2007, CUP E62I15000330002).

Competing interests

The authors declare that they have no competing interests.

Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

Authors’ Affiliations

(1)
Department of Veterinary Medicine and Animal Productions, Università di Napoli Federico II

References

  1. Kaakoush NO, Castaño-Rodríguez N, Mitchell HM, Man SM. Global epidemiology of Campylobacter infection. Clin Microbiol Rev. 2015;28:687–720.View ArticlePubMedPubMed CentralGoogle Scholar
  2. Newell DG, Fearnley C. Sources of Campylobacter colonization in broiler chickens. Appl Environ Microbiol. 2003;69:4343–51.View ArticlePubMedPubMed CentralGoogle Scholar
  3. Dipineto L, Gargiulo A, De Luca Bossa LM, Rinaldi L, Borrelli L, Menna LF, Fioretti A. Prevalence of thermotolerant Campylobacter in pheasants (Phasianus colchicus). Avian Pathol. 2008;37:507–8.View ArticlePubMedGoogle Scholar
  4. Dipineto L, Gargiulo A, De Luca Bossa LM, Rinaldi L, Borrelli L, Santaniello A, et al. Prevalence of thermotolerant Campylobacter in partridges (Perdix perdix). Lett Appl Microbiol. 2009;49:351–3.View ArticlePubMedGoogle Scholar
  5. Gargiulo A, Sensale M, Marzocco L, Fioretti A, Menna LF, Dipineto L. Campylobacter jejuni, Campylobacter coli, and cytolethal distending toxin (CDT) genes in common teals (Anas crecca). Vet Microbiol. 2011;150:401–4.View ArticlePubMedGoogle Scholar
  6. Sifré E, Salha BA, Ducournau A, Floch P, Chardon H, Mégraud F, Lehours P. EUCAST recommendations for antimicrobial susceptibility testing applied to the three main Campylobacter species isolated in humans. J Microbiol Methods. 2015;119:206–13.View ArticlePubMedGoogle Scholar
  7. López CM, Giacoboni G, Agostini A, Cornero FJ, Tellechea DM, Trinidad JJ. Thermotolerant Campylobacters in domestic animals in a defined population in Buenos Aires, Argentina. Prev Vet Med. 2002;55:193–200.View ArticlePubMedGoogle Scholar

Copyright

© The Author(s) 2017

Advertisement