ABSTRACT
Campylobacter species cause human gastrointestinal infections worldwide. They commonly inhabit intestines of avian species including wild birds. They might play a role in the spread of infections to humans and other bird species. The prevalence of Campylobacter species in 2164 faecal samples of wild birds (representing 71 species and 28 families) captured across the Korean peninsula was evaluated in this study. The overall prevalence was 15.3% (332/2164). Bird species belonging to the family Charadriidae had the highest isolation rate (30.0%), followed by those belonging to the families Ardeidae (26.4%), Turdidae (21.9%), and Anatidae (15.3%). The prevalence of Campylobacter spp. differed significantly according to migratory habit. Stopover birds were the most commonly infected (19.0%), followed by winter migratory (16.7%) and summer migratory birds (12.3%). However, indigenous birds showed very low prevalence (2.7%). Antimicrobial susceptibility tests were performed for 213 isolates. Results showed that Campylobacter jejuni isolates (n = 169) exhibited resistance to nalidixic acid (5.3%), ciprofloxacin (3.0%), and tetracycline (1.8%), while Campylobacter lari (n = 1) displayed resistance to nalidixic acid and ciprofloxacin. However, all Campylobacter coli isolates (n = 20) were susceptible to all antimicrobials tested. This is the first report on the prevalence of Campylobacter species in wild birds that seasonally or indigenously inhabit the Korean peninsula. Our results indicate that the overall prevalence of Campylobacter in wild birds is moderate. Therefore, birds might serve as significant reservoirs for Campylobacter pathogens.
Introduction
Infection with Campylobacter species continues to be a leading cause of human infectious intestinal disease worldwide with significant social and economic impacts (Allos, Citation2001; Roberts et al., Citation2003). Campylobacter species have been readily isolated from a variety of environmental and animal sources. They are well-adapted to survive in avian species (Petersen et al., Citation2001; Waldenstrom et al., Citation2002; French et al., Citation2005). In most human cases of diseases caused by Campylobacter species, outbreaks are associated with foods or contaminated environment, although it is very difficult to trace the source of contamination (Frost, Citation2001; Hanninen et al., Citation2003; Colles et al., Citation2008; Medeiros et al., Citation2008). In particular, a large proportion of human cases are considered to be caused by the consumption of contaminated chicken meat (Frost, Citation2001; Baker et al., Citation2006; Colles et al., Citation2008).
Wild birds have been considered as natural reservoirs of Campylobacter species (Kapperud & Rosef, Citation1983). They are frequently described as potential sources of Campylobacter infection in humans, farm animals, and poultry (Rosef et al., Citation1985; Southern et al., Citation1990; Hanninen et al., Citation1998; Studer et al., Citation1999). Nevertheless, only limited information on the prevalence of Campylobacter in wild birds is available, although its prevalence has been well defined in humans and chickens (Gregory et al., Citation1997; Petersen et al., Citation2001; Waldenstrom et al., Citation2002; Hughes et al., Citation2009; Ku et al., Citation2011). A better understanding of the epidemiology and ecology of Campylobacter in wild birds is needed to determine the risk of transmission of Campylobacter species to humans and domestic animals.
In this study, a large nationwide survey of wild bird populations in the Korean peninsula was undertaken to investigate the prevalence of Campylobacter species. Most previous studies on the epidemiology of Campylobacter in wild birds have been focused on a narrow range of bird species or habitats, although some studies have examined a broad range of species or conducted nationwide surveys (Yogasundram et al., Citation1989; Quessy & Messier, Citation1992; Waldenstrom et al., Citation2002; Hughes et al., Citation2009). Therefore, the objective of this study was to investigate the host range and prevalence of Campylobacter spp. in wild bird populations in Korea and determine if there was any relationship between their host range and prevalence and taxa and migratory patterns of these birds (either seasonally migratory or indigenous). In addition, antimicrobial resistance of these isolates obtained from birds was evaluated in this study.
Materials and methods
Wild bird sampling
Wild birds were sampled from 2009 to 2010 in summer and winter seasons. In the summer season (from April to September 2009), most summer migratory birds, stopover birds, and indigenous birds were sampled. Sampling for winter migratory birds was conducted in the winter season (between October 2009 and March 2010). Birds were captured near roadside vegetation, crop fields, creeks and ponds, and observed shrubs including major wild bird habitats with mist nets and walk-in traps (Kang et al., Citation2010). Each captured bird was sequentially identified, marked, sampled, and released. Faecal samples were collected by swabbing the cloaca or by collecting fresh faeces from birds during capture and restraint using BBL CultureSwab™ and collection device (Beckton, Dickinson and Company, Sparks, MD, USA). Permission to capture wild birds was given by the Ministry of Environment and Cultural Heritage Administration, Republic of Korea. The samples were transported to our laboratory within 24–48 h in a refrigerated container and stored at 4°C until use.
Bacterial culture
Each swab or 1 g of each faecal sample taken from wild birds was pre-enriched in 10 ml of Preston Campylobacter selective enrichment broth (Oxoid, Basingstoke, Hampshire, England) at 42°C for 48 h in a jar with a microanaerobic gas mixture of 6% O2, 7.1% CO2, 3.6% H2, and 83.3% N2 using an Anoxomat system (Mart Microbiology B.V., Drachten, Netherlands). A loopful of the pre-enriched broth was streaked onto charcoal cefoperazone deoxycholate agar (Oxoid). The plates were incubated at 42°C for 48 h under microanaerobic conditions. Bacterial colonies (3–5 colonies/bird) grown on the charcoal cefoperazone deoxycholate agar (Oxoid) medium were used to identify Campylobacter species following oxidase and catalase tests.
Molecular identification of Campylobacter species by polymerase chain reaction
DNA extraction was performed for each isolate by boiling the colonies for 10 min and centrifuging at 13,000 x g for 10 min. The isolates were initially identified as Campylobacter spp. by polymerase chain reaction (PCR) of the 16S rRNA gene as described previously elsewhere (Lawson et al., Citation1998). Campylobacter isolates were identified to be Campylobacter jejuni, Campylobacter coli, or Campylobacter lari using a multiplex PCR targeting hipO and 23S rRNA genes of C. jejuni and the glyA gene of C. coli and C. lari as described previously (Wang et al., Citation2002). After the initial 16S rRNA gene PCR, the isolates were frozen at –80°C in 15% glycerol broth (Oxoid). One isolate per species per bird was used to determine the prevalence of Campylobacter species in the birds and their antimicrobial susceptibility.
Antimicrobial susceptibility testing
Antimicrobial susceptibilities were tested according to the procedure described by Buck & Kelly (Citation1982). Minimum inhibitory concentrations (MICs) were determined with the 96-well microplate dilution method using Mueller–Hinton broth (Oxoid). MIC breakpoints for resistance were as follows: azithromycin (AZM), ≥8 µg/ml; ciprofloxacin (CIP), ≥4 µg/ml; erythromycin (ERY), ≥32 µg/ml; gentamicin (GEN), ≥8 µg/ml; tetracycline (TET), ≥16 µg/ml; florfenicol (FLR), ≥8 µg/ml; nalidixic acid (NAL), ≥64 µg/ml; telithromycin (TEL), ≥16 µg/ml; and clindamycin (CLI), ≥8 µg/ml (CLSI, Citation2010; FDA, Citation2012). MICs of all antimicrobial agents tested for each isolate were recorded after 48 h of incubation at 37°C under a microaerophilic atmosphere.
Results
During 2009–2010, 2164 birds representing 71 species in 28 families including Anatidae, Ardeidae, Charadriidae, Corvidae, Scolopacidae, and Turdidae were sampled. Campylobacter isolates were recovered from faecal samples of 332 wild birds belonging to 30 species in 8 families. Overall, the prevalence of Campylobacter in birds was 15.3% (). None of these birds tested positive for Campylobacter showed any obvious external disease signs. By bird family, the highest prevalence was 30% (9/30) in Charadriidae, followed by 26.4% (9/34) in Ardeidae, 21.9% (9/41) in Turdidae, 15.3% (252/1,642) in Anatidae, and 15.1% (15/99) in Scolopacidae. By bird species, the isolation rate of Campylobacter in grey plover (Pluvialis squatarola) was 100% (3/3). It was 100% (1/1) in black-tailed gull (Larus crassirostris), 100% (1/1) in Ruddy turnstone (Arenaria interpres), 100% (1/1) in green sandpiper (Tringa ochropus), 100% (2/2) in Far Eastern curlew (Numenius madagascariensis), 80% (4/5) in little egret (Egretta garzetta), 52.2% (46/88) in European wigeon (Anas Penelope), and 50% (2/4) in falcated duck (Anas falcata).
Table 1. The prevalence of Campylobacter spp. in different species of wild birds in South Korea.
Based on migratory habits, the following four types of birds were found in the Korean peninsula: 12 winter migratory bird species (1712 birds); 20 summer migratory bird species (146 birds); 18 passage bird species (121 birds); and 21 indigenous bird species (185 birds). Overall, birds of seasonally migratory type or passage birds showed higher rates of Campylobacter infection than indigenous birds. Passage birds such as plovers and curlew had the highest prevalence of Campylobacter spp. (19.0%, 23/121), followed by winter migratory birds (16.7%, 286/1712) mainly belonging to the family Anatidae, and summer migratory birds including egrets, herons, and thrushes (12.3%, 18/146). Among 185 individuals classified as indigenous birds, Camplyobacter spp. were only isolated from five birds (2 magpies, 1 gull, 1 sandpiper, and 1 sanderling) with a prevalence of 2.7%.
We were unable to recover all Campylobacter isolates from glycerol stocks of isolates from 332 birds for species identification. Consequently, species-specific PCR assays identified a total of 213 isolates (one isolate per species per bird) for further characterization. Of the 213 Campylobacter spp. isolates, C. jejuni was identified the most frequently (79.3%, 169/213), followed by C. coli (9.3%, 20/213) and C. lari (0.4%, 1/213). Other Campylobacter spp. were detected at a frequency of 10.7%. Interestingly, 20 C. coli isolates were obtained from three bird species (18 isolates from Picus canus, 1 isolate from Anas acuta, and 1 isolate from A. penelope), whereas C. jejuni was frequently identified in a wide range of bird species.
Also, the 213 Campylobacter spp. isolates obtained from wild birds were subjected to antimicrobial susceptibility tests. MICs of AZM, CIP, ERY, GEN, TET, FLR, NAL, TEL, and CLI were in ranges of 0.03–0.25, 0.03–16, 0.06–4, 0.12–1, 0.12–64, 0.5–4, 4–64, 0.12–4, and 0.12–1 µg/ml, respectively (). All isolates were found to be susceptible to AZM, ERY, ERY, GEN, FLR, TEL, and CLI. Of C. jejuni isolates (n = 169), nine (5.3%) were resistant to NAL, five (3.0%) were resistant to CIP, and three (1.8%) were resistant to TET. The isolate of C. lari (n = 1) displayed resistance to NAL and CIP. All C. coli isolates (n = 20) were susceptible to all antimicrobials tested. Regarding other Campylobacter spp. isolates (n = 23), only one (4.3%) of them showed resistance to NAL.
Table 2. MIC values of antimicrobial agents tested for 213 Campylobacter isolates from wild birds for 2009–2010.
Discussion
The present study showed that the overall prevalence of Campylobacter in wild birds sampled around the Korean peninsula was 15.3%. This prevalence can be considered as a moderate level compared to that (ranging from 2% to 50%) in wild birds reported in other studies (Waldenstrom et al., Citation2002; Hughes et al., Citation2009). Because the detection rate of 15.3% in the present study was based on cultural detection of Campylobacter, a higher detection rate might be obtained if PCR was performed directly for faecal samples. We also found that the distribution of Campylobacter spp. was highly different among bird taxa and migratory habits. In two previous studies, the prevalence of Anatidae is 27% in Europe and 2% in the USA (Waldenstrom, Citation2005; Keller et al., Citation2011). In the present study, Campylobacter was detected in 15.3% of Anatidae bird samples. There were also differences in the prevalence of Campylobacter in Turdidae: 21.9% prevalence in Korea, 14% in Europe, and 3% in the USA. Although the reason for these differences in the prevalence of Campylobacter among those regions is currently unclear, regional ecological factors such as habitat and diet as well as body condition and health of birds might have resulted in such differences. The detection method might have also influenced the rate of detection because Campylobacter is sensitive to suboptimal storage and culture conditions of samples (Lawson et al., Citation1998; Van Dyke et al., Citation2010).
It has been reported that C. jejuni is the most prevalent Campylobacter species isolated from wild birds (particularly waterfowl), although C. coli and C. lari are also isolated (Colles et al., Citation2008; Hughes et al., Citation2009; Van Dyke et al., Citation2010; Keller et al., Citation2011). For example, previous studies have revealed that most (73%) wild waterfowls including seagull, ducks, and Canada geese in southern Ontario, Canada, harbour C. jejuni, while 13% and 27% of them harbour C. coli and C. lari, respectively (Van Dyke et al., Citation2010). For wild geese in Oxfordshire, United Kingdom, 50.2% of them harbour C. jejuni, while 0.3% and 0% of them harbour C. coli and C. lari, respectively (Colles et al., Citation2008). For wild birds in the mid-Atlantic region of the USA, 7.2%, 0%, and 0% of them harbour C. jejuni, C. coli, and C. lari, respectively (Keller et al., Citation2011). In the present study, C. jejuni was isolated from 7.8% of wild birds. This percentage might have been underestimated due to the exclusion of isolates that were unavailable for species identification. Nevertheless, C. jejuni was the most common species of Campylobacter isolated from wild birds in South Korea, accounting for 79.3% of the isolates. C. jejuni, C. coli, and C. lari are the most frequently isolated species from humans. However, C. jejuni is the main cause of human infections. It accounts for more than 90% of cases (Frost, Citation2001; Gillespie et al., Citation2002; Van Dyke et al., Citation2010). Therefore, the high prevalence of C. jejuni in wild birds worldwide indicates that this organism is well-adapted to wild bird species. It poses a potential risk to public health. Further studies using molecular subtyping methods such as pulsed-field gel electrophoresis and multi-locus sequence typing are needed to better assess the public health significance of these wild bird isolates (Frost, Citation2001; Hughes et al., Citation2009).
A number of studies have reported the antimicrobial resistance of Campylobacter in humans and birds, many of which have much higher resistance than those found in this study (Aarestrup & Engberg, Citation2001; Luangtongkum et al., Citation2009). For instance, of C. jejuni isolates from Dutch humans and poultry in 1992 and 2004, 15% and 35% of them are resistant to fluoroquinolones, respectively (van Hees et al., Citation2007). In France, of C. jejuni isolates from humans and broilers in 2004, 25.3% and 9.4% are resistant to fluoroquinolones, respectively (Gallay et al., Citation2007). Moreover, it has been reported that Campylobacter spp. isolated from domestic chicken meat and humans in South Korea are highly resistant to antimicrobials (Hong et al., Citation2007; Ku et al., Citation2011; Wei et al., Citation2015). Ku et al. (Citation2011) have reported that 82.3% of human isolates and more than 90% of domestic chicken meat isolates of Campylobacter have multidrug resistances (MDRs), and 82.3% and 95% of them are resistant to fluoroquinolones, respectively. Hong et al. (Citation2007) have also reported that more than 84% of Campylobacter species isolated from retail raw meat including chicken meat in South Korea are resistant to fluoroquinolones and 93% of these isolates have MDRs. More recently, Wei et al. (Citation2015) have revealed that fluoroquinolone-resistant MDR Campylobacter is disseminated in wild birds such as terrestrial birds, shore birds, and waterfowl in South Korea. In contrast, resistance to antimicrobial agents in wild bird isolates of Campylobacter was found to be very low in the present study. The resistance rate of C. jejuni isolates to fluoroquinolones was 3%, similar to that observed in wild birds in Sweden (0.7%) (Waldenstrom et al., Citation2005). Although resistance rates are very low, wild birds cannot be naturally exposed to fluoroquinolones. Therefore, these wild birds may have been infected by fluoroquinolone-resistant Campylobacter which acquired resistance in the intestines of industrial animals treated by fluoroquinolones. Also, Campylobacter species originally inhabiting birds’ intestines might have acquired resistance through acquiring resistance genes from other organisms. Molecular epidemiological analyses are needed to provide a better insight into ecological factors associated with the transmission of Campylobacter between wild birds and their environments or other host species.
This study is the first one that reports the prevalence of Campylobacter species in wild birds that seasonally or indigenously inhabit the Korean peninsula. Such information has not been reported in the literature. Our findings indicate that there is an overall moderate prevalence of Campylobacter in wild birds, particularly in waterfowls, demonstrating that these wild birds might serve as significant reservoirs for Campylobacter pathogens. Further studies are needed to correctly assess the impact of wild birds on the epidemiology of Campylobacter infections in the near future. Genetic analysis of various isolates from domestic and wild birds and those from humans within South Korea is needed using DNA-based typing methods such as pulsed-field gel electrophoresis and multi-locus sequence typing (Frost, Citation2001; Hughes et al., Citation2009).
Acknowledgements
We thank Mi-Jin Kim for technical assistance.
Disclosure statement
No potential conflict of interest was reported by the authors.
Additional information
Funding
References
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