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Applied and Environmental Microbiology, December 2002, p. 5911-5917, Vol. 68, No. 12
0099-2240/02/$04.00+0     DOI: 10.1128/AEM.68.12.5911-5917.2002
Copyright © 2002, American Society for Microbiology. All Rights Reserved.

Prevalence of Campylobacter jejuni, Campylobacter lari, and Campylobacter coli in Different Ecological Guilds and Taxa of Migrating Birds

Jonas Waldenström,^1,2 Tina Broman,^3,4 Inger Carlsson,⁵ Dennis Hasselquist,¹ René P. Achterberg,⁶ Jaap A. Wagenaar,⁶ and Björn Olsen^2,3,7*

Department of Animal Ecology, Lund University, SE-223 62 Lund,¹ Department of Infectious Diseases,³ Department of Molecular Biology, Umeå University, SE-901 87 Umeå,⁴ Department of Clinical Microbiology, Kalmar County Hospital, SE-391 85 Kalmar,⁵ Research Institute for Zoonotic Ecology and Epidemiology (RIZEE),SE-396 93 Färjestaden,⁷ Ottenby Bird Observatory, SE-380 65 Degerhamn, Sweden,² Division of Infectious Diseases and Food Chain Quality, Institute for Animal Science and Health (ID-Lelystad), 8200 AB Lelystad, The Netherlands⁶

Received 26 March 2002/ Accepted 30 August 2002

Top Abstract Introduction Materials and Methods Results Discussion References

 
A total of 1,794 migrating birds trapped at a coastal site in southern Sweden were sampled for detection of Campylobacter spp. All isolates phenotypically identified as Campylobacter jejuni and a subset of those identified as non-C. jejuni were identified to the species level by PCR-based techniques. C. jejuni was found in 5.0% of the birds, Campylobacter lari was found in 5.6%, and Campylobacter coli was found in 0.9%. An additional 10.7% of the tested birds were infected with hippurate hydrolysis-negative Campylobacter spp. that were not identified to the species level. The prevalence of Campylobacter spp. differed significantly between ecological guilds of birds. Shoreline-foraging birds feeding on invertebrates and opportunistic feeders were most commonly infected (76.8 and 50.0%, respectively). High prevalence was also shown in other ground-foraging guilds, i.e., ground-foraging invertebrate feeders (11.0%), ground-foraging insectivores (20.3%), and plant-eating species (18.8%). Almost no Campylobacter spp. were found in ground-foraging granivores (2.3%), arboreal insectivores (0.6%), aerial insectivores (0%), or reed- and herbaceous plant-foraging insectivores (3.5%). During the autumn migration, a high proportion of samples from juveniles were positive (7.1% in passerines, 55.0% in shorebirds), indicating transmission on the breeding grounds or during the early part of migration. Prevalence of Campylobacter spp. was associated with increasing body mass among passerine bird species. Furthermore, prevalence was higher in short-distance migrants wintering in Europe than in long-distance migrants wintering in Africa, the Middle East, or Asia. Among ground-foraging birds of the Muscicapidae, those of the subfamily Turdinae (i.e., Turdus spp.) showed a high prevalence of Campylobacter spp., while the organism was not isolated in any member of the subfamily Muscicapinae (i.e., Erithacus and Luscinia). The prevalence of Campylobacter infection in wild birds thus seems to be linked to various ecological and phylogenetic factors, with great variations in carriership between different taxa and guilds.

Top Abstract Introduction Materials and Methods Results Discussion References

 
For decades, wild birds have been considered natural vertebrate reservoirs of Campylobacter spp. (23, 25) and are frequently mentioned as possible vectors for transmission to poultry (2, 15, 40), cattle (22), and humans (35, 38, 44). Campylobacter jejuni, the main human pathogen of the genus, is now recognized as a leading cause of acute bacterial gastroenteritis in many parts of the world (3, 18). Understanding the epidemiology of Campylobacter spp. in wild birds appears to be an essential part of the puzzle. However, although the prevalence of Campylobacter spp. in humans and poultry has been well studied (2, 3), little is known about the prevalence of this organism in wild birds. Published works on wild birds in the context of Campylobacter epidemiology have focused either on single taxonomic groups of birds, e.g., wildfowl (27, 29), shorebirds (19), gulls (26, 45), and corvids (38), or on birds inhabiting different habitats, e.g., rural and urban areas (20, 24, 25). The few studies examining a broad spectrum of species (25, 30, 46) lack systematic sampling procedures, possibly resulting in biased interpretation of the data.

To overcome these problems, we conducted standardized sampling of a large number of individuals and species of wild birds at a single migration locality over an entire season (March to November). Our goals were to determine in which groups of wild birds the different Campylobacter spp. were present and to reveal which ecological parameters influenced the prevalence of infection. The present study offers the largest survey to date of the prevalence of Campylobacter spp. in migratory birds (1,794 individuals from 107 species), providing a unique data set for giving new insights into the ecology and epidemiology of this host-parasite interaction.

Top Abstract Introduction Materials and Methods Results Discussion References

 
Sampling procedures and measurements.
Fieldwork was conducted at Ottenby Bird Observatory (56°12'N, 16°24'E), on the southernmost point of the island Öland in southeastern Sweden. Passerines were trapped with mist nets and Helgoland traps (6) in the bird observatory garden, and shorebirds were trapped with Ottenby funnel traps (6) on the shoreline surrounding the point. Captured birds were banded, weighed, and measured and their ages were determined according to differences in feather shape and wear (4, 33, 41), enabling separation of juvenile and adult birds in autumn and yearling and adult birds in spring.

Birds migrating through Ottenby breed mostly in Sweden, Finland, and Russia (1). All trapped birds except jackdaws (Corvus monedula) were regarded as migrants, since the observatory garden offers only limited breeding possibilities. Every 10th bird banded during the studied migration periods, 25 March to 15 June 2000 (spring migration) and 1 July to 15 November 2000 (autumn migration), was sampled for the prevalence of Campylobacter spp. During days on which more than 500 birds were trapped (>500 birds, n = 5), the sampling was less intense. Species normally trapped only in small numbers at Ottenby (<10 individuals per year) were sampled in higher proportions.

Two different approaches were used to obtain fecal samples, depending on the size of the trapped bird. Smaller birds were put in a dark box one by one with a clean sheet of paper at the bottom. After the bird had defecated (normally after 5 to 10 min), the fecal sample was placed in charcoal transport medium (Transwab; BioDisc, Solna, Sweden) and stored at refrigerator temperature until cultivation. Large birds, i.e., those with a body mass exceeding 250 g, were sampled by insertion of a sterile swab 1 to 2 cm into the cloaca.

Laboratory analyses.
Samples were cultivated at the Department of Clinical Microbiology at Kalmar County Hospital by methods routinely used for clinical samples. Each sample was plated onto a Campylobacter-selective, blood-free medium (45.5 g of Campylobacter-selective agar base LAB M/LAB 112 per liter, 2 ampoules of cefoperazone-amphotericin supplement LAB M/X 112; Lab M, Bury, England). Incubation was performed at 42°C in a microaerobic atmosphere (85% N_2, 10% CO₂, 5% O₂). Plates were examined after 48 and 72 h. Isolates with gram-negative gull-shaped cells (identified by light microscopy at a magnification of x1,000), positive reactions in catalase and oxidase tests, and inability to grow under aerobic conditions at 37°C were regarded as Campylobacter spp. Cultures were frozen at -80°C in broth (75% horse serum, 75 g of glucose BDH 10117 4Y/liter, 1.25 g of Lab Lemco Oxoid L29/liter, 2 g of Bacto Peptone [Difco catalog no. 0118-15]/liter). Due to the large number of samples to be analyzed, no enrichment step was included as this would have obstructed fulfillment of the entire study. Further, the sampling scheme was in operation every day during the field season, including holidays and weekends, and therefore not all samples could be analyzed on the date of collection. The majority of samples were analyzed within 48 h after sampling, while a few were analyzed up to 4 days after collection. However, previous testing of our methods showed good recovery of Campylobacter spp. even 5 days after sampling (data not shown).

The isolates were subjected to a hippurate hydrolysis test, and all isolates with positive reactions were further analyzed by one of two genotypic tests for confirmation of species identification. A PCR directed at the 23S rRNA gene identified isolates as being thermotolerant Campylobacter spp. Subsequent endonuclease digestion of the PCR products produces species-specific fragment patterns (17). In short, the PCR mixture contained 0.25 µM (each) primers THERM1 and THERM4 (17), 50 mM KCl, 10 mM Tris-HCl, 1.5 mM MgCl₂, 0.1 mM each deoxynucleotide, and 0.02 U of AmpliTaq Gold (PE Applied Biosystems, Branchburg, N.J.). An initial denaturing step of 12 min at 94°C to activate the AmpliTaq enzyme started the PCR, followed by 45 cycles with a thermal profile of 94°C for 1 min, 56°C for 1 min, and 72°C for 1 min, followed by a final extension step of 72°C for 10 min. Species determination was performed through digestion of 10 µl of the PCR products with 0.5 U of AluI for 1 h and subsequent separation of digestion products on agarose gels. Banding patterns were compared to those produced by type strains of C. jejuni, Campylobacter coli, and Campylobacter lari. The second method used for species identification is a multiplex PCR with primer pairs specific for C. jejuni and C. coli (43). We followed the protocol of Vandamme et al. (43) but performed the reaction with 25-µl volumes instead of 50-µl volumes. Boiled lysates or purified DNA (Puregene DNA isolation kit; Gentra Systems, Minneapolis, Minn.) was used as the template for both methods, and reference strains of C. jejuni, C. coli, and C. lari were used as controls. A subset (106 of 295 isolates) of the hippurate hydrolysis-negative isolates was genetically characterized by using a published PCR-restriction fragment length polymorphic analysis protocol (28). The template DNA used in this method was isolated as described previously (16). In short, material from one colony was mixed with 300 µl of a 20% Chelex-100 suspension in Tris-EDTA buffer and heated for 10 min at 95°C. After centrifugation, the supernatant was used as the template in the PCRs. The restriction patterns obtained in the PCR-restriction fragment length polymorphic analysis were visually compared to patterns obtained from 43 reference strains, including C. coli (4), Campylobacter fetus (2), Campylobacter helveticus (1), Campylobacter hyointestinalis (5), C. jejuni (5), C. lari (6), Campylobacter mucosalis (1), Campylobacter sputorum (3), Campylobacter upsaliensis (5), and Arcobacter (11). Reference strains were obtained from the American Type Culture Collection (C. fetus) and the BCCM/LMG collection (Ghent, Belgium).

Top Abstract Introduction Materials and Methods Results Discussion References

 
Out of 21,666 birds banded, a total of 1,794 individual birds (representing 107 species from 26 families) were tested for the presence of Campylobacter spp. (425 individuals in spring and 1,369 individuals in autumn) (Table 1). C. jejuni was isolated from 89 birds (13 in spring, 76 in autumn), C. lari was isolated from 100 birds (4 in spring, 96 in autumn), and C. coli was isolated from 17 birds (7 in spring, 10 in autumn). An additional 192 isolates from birds (all in autumn) were phenotypically assigned to the hippurate hydrolysis-negative Campylobacter spp. but were not identified to the species level by genotypic methods (Table 1). Ten birds had concomitant infections with C. jejuni and C. coli. Two isolates were identified as thermotolerant Campylobacter spp. by the 23S rRNA methods of Fermér and Engvall (17) but gave aberrant patterns after restriction enzyme digestion and were therefore regarded as nontypeable. The mean prevalence of Campylobacter infection was 21.6% for all tested birds but varied from 0 to 100% between species (Table 1). In total, Campylobacter spp. were recorded in 13 out of 26 bird families investigated. C. jejuni was isolated from nine families, C. coli was isolated from two families, and C. lari was isolated from six families (Table 1). These figures must be regarded as minimum values as die-off of campylobacters during transport could have occurred. Also, as no enrichment was used, low numbers of organisms may have gone undetected. Furthermore, the growth conditions used in this study preclude growth of Campylobacter species that require anoxic environments or the presence of H₂.

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TABLE 1. Birds tested for presence of Campylobacter spp.

Campylobacter-positive samples were obtained from 72 juvenile birds of 24 species during the autumn migration (C. jejuni, 36 individuals of 14 species; C. lari, 7 individuals of 4 species; C. coli, 1 individual; hippurate hydrolysis-negative Campylobacter spp., 26 individuals of 18 species; nontypeable, 2 individuals of 2 species). Positive samples originated from a variety of families, namely, Sylviidae, Regulidae, Paridae, Passeridae, Fringillidae, Anatidae, Muscicapidae, Sturnidae, Accipitridae, Strigidae, Scolopacidae, and Certhidae. We compared the two most frequently sampled bird groups, passerines and shorebirds, in more detail. In passerines, 7.1% of juveniles (n = 676) and 6.1% of adults (n = 115; ^{2₁ = 0.31, P = 0.58) tested positive for Campylobacter spp., compared to 55.0% of juvenile (n = 20) and 75.8% of adult (n = 364; 2₁ = 4.35, P = 0.04) shorebirds.}

The size of the bird might be related to the probability of its carrying a Campylobacter infection if, for example, large and small birds differ in their habits, habitat preferences, or distributions. We calculated the mean body mass for each passerine species and divided the species into two groups, infected and uninfected. We calculated the mean values for each species in each group and tested the difference between the two groups with a t test. The value for uninfected species was 19.3 g (standard deviation [SD] = 13.6), significantly lower than 52.2 g (SD = 56.4) for the infected species (t test, t = 3.85, P < 0.001, n = 50 uninfected species and 16 infected species). Among shorebirds, the difference in mean body mass between infected and uninfected species was lower than that for passerines, 85.4 g in infected species and 88.6 g in uninfected species. However, among shorebirds, the uninfected species group was comprised of only 3 of the 19 species (Table 1), and less than three individuals were sampled for each of these 3 uninfected species, thus precluding further statistical treatment.

We compared prevalence rates to distance of migration for all species not directly associated with water (i.e., shorebirds, gulls, ducks, and rails were excluded), with the birds divided into two groups. The first group was made up of short-distance migrants (birds migrating to different parts of Europe), while the second group was made up of long-distance migrants (birds migrating to Africa, the Middle East, or Asia). Among long-distance migrants, only 13 (3%) individuals representing 4 species tested positive for Campylobacter spp., out of 426 tested birds of 36 species. In contrast, 76 (11%) of the short-distance migrants tested positive, representing 16 species out of 716 tested birds of 43 species. These differences were significant both for number of infected species (^{2₁ = 7.06, P = 0.008) and number of infected individuals (2₁ = 21.26, P < 0.001).}

The prevalence of Campylobacter spp. in different ecological guilds is shown in Table 2, where birds are divided into groups according to their main foraging habits (7, 8, 9, 10, 11, 12, 13, 14). Almost no Campylobacter spp. were found in granivores or insectivores. Most guilds that forage at ground level showed high prevalence rates; also, raptors and opportunistic feeders were often infected by Campylobacter spp. (Table 2). We tested for statistical association between feeding preference, i.e., feeding mainly in water or on land, and the Campylobacter type isolated from the bird species. Of 12 species from which C. lari was isolated, 8 species normally feed in water, and among 19 species from which C. jejuni was isolated, 13 species preferably feed on land (^{2₁ = 3.66, P = 0.06). C. lari was isolated more frequently in nonpasserine individuals (30.5% of positive samples, n = 279) than in passerine individuals (16.3% of positive samples, n = 49; 2₁= 33.05, P < 0.001), and there was a tendency for this to occur at the species level (passerine species, 25.0% of positive samples, n = 16; nonpasserine species, 50.0%, n = 16; 2₁ = 2.13, P = 0.14).}

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TABLE 2. Prevalence of Campylobacter spp. in different ecological guilds

Top Abstract Introduction Materials and Methods Results Discussion References

 
Overall, we found a high frequency of Campylobacter spp. in migrating birds (21.6%). However, the distribution of Campylobacter among bird taxa and guilds was very heterogeneous. Certain bird taxa had high prevalences, e.g., shorebirds (Scolopacidae and Charadridae, 79.6%), wagtails and pipits (Motacillinae, 25.0%), starlings (Sturnidae, 40.0%), and thrushes (Turdinae, 37.9%), while others did not (Table 1). Among the Turdinae, Campylobacter infection was found only in Turdus individuals, while Erithacus, Luscinia, Oenanthe, Saxicola, and Phoenicurus individuals tested negative. It is interesting to note that these results coincide with new phylogenetic classifications of the thrushes based on comparisons of genetic material. These new classifications place thrushes into two different subfamilies of the Old World flycatcher family (Muscicapidae). Turdus is placed in the subfamily Turdinae, while Erithacus, Oenanthe, Luscinia, and Phoenicurus are placed together with Ficedula and Muscicapa in the subfamily Muscicapinae (36, 37). Thus, in our study, all species of the Muscicapinae were free of Campylobacter, while almost all species of the Turdinae carried Campylobacter (Table 1). Why Turdus had such a high prevalence of Campylobacter while Erithacus had none seems to be an important question that we, unfortunately, can only ask, not answer. Although both genera forage on the ground for invertebrates, perhaps there are subtle ecological differences in microhabitat use, foraging habits, or diet that result in Turdus being exposed to Campylobacter more often than Erithacus. Another possible answer is that some evolutionary change in the birds of the subfamily Muscicapinae has resulted in that lineage being more resistant to Campylobacter than the Turdinae.

The prevalence of Campylobacter spp. was highly influenced by feeding habits. In some ecological guilds, e.g., most types of insectivores and granivores, Campylobacter spp. were rarely or never isolated. However, in other guilds, i.e., in raptors, in opportunistic feeders, and in most ground-foraging guilds, prevalence was found to be high.

The positive relationship between the prevalence of Campylobacter spp. and increasing body mass among the passerine bird species may have several plausible explanations. Body mass is positively correlated with longevity in passerines (5, 21), and a longer life span would increase the number of potential transmission contacts, resulting in a higher risk of contracting the bacteria. However, a large proportion of juvenile birds were already infected on their first autumn migration, at an age of 1 to 4 months, implying that transmission had already taken place on the breeding grounds, or at stopover sites during early stages of the autumn migration, indicating that age may not be so important a factor. In shorebirds, however, Campylobacter isolation was more frequent in adult individuals but the number of sampled juveniles was far less than that of adults.

Based on our knowledge of Campylobacter survival in the environment (42), and reports of isolation of these bacteria from surface water (22, 39), it is reasonable to assume that the habitats preferred by different bird species may result in different levels of exposure to Campylobacter. There was a tendency for isolation rates of C. jejuni to differ from those of C. lari when the main foraging habitat of the species was considered. However, within the data set, there was a statistically significant difference in isolation of C. lari from nonpasserine individuals and in isolation of C. jejuni from passerines. At the host species level, this difference was not significant, but it probably would have been if all hippurate hydrolysis-negative Campylobacter spp. had been identified to the species level genetically, since nearly all of those tested proved to be C. lari.

Shorebirds differ in several aspects from passerines. They generally have a longer life span (11), are often gregarious, feed side by side in mixed-species flocks, and feed at water edges or in shallow waters of habitats that commonly harbor Campylobacter spp., e.g., at river mouths, seashores, and sewage plants. The frequent utilization of these kinds of habitats by shorebirds is a likely explanation for the high overall prevalence of Campylobacter spp. in this type of birds, especially since feeding activities would be the most likely route through which the birds would become exposed to the bacteria.

Are Campylobacter spp. a commensal of avian intestines? The growth temperature range of these bacteria, which fits the body temperature of birds rather than that of mammals (34), suggests that the answer is yes. Furthermore, in this study and in several other studies, high prevalences of C. jejuni, C. coli, and C. lari were found in apparently healthy birds (25, 29). High isolation rates could, in our opinion, be interpreted as evidence for a nonharmful coexistence between Campylobacter species and their bird hosts, indicating a long evolutionary history of host-parasite interactions. Certain strains of the bacteria might have coevolved with certain bird species, possibly protecting the host against invasion by more harmful strains. Accordingly, the finding of certain bird species with low or no prevalence of the bacteria may reflect an inability of the bacterium to maintain an infection. Alternatively, it might reflect that birds generally have a strong immune system, developed to eliminate Campylobacter infections or to reduce them to a level undetectable by the methods used in this study. It is not known if, or to what extent, wild birds are affected by infection with Campylobacter spp. nor for how long infection is maintained in a bird.

We do not know if the Campylobacter isolates found in this study are transmissible to humans or domesticated animals, but there might nevertheless be some epidemiological considerations. Given the occurrence of C. jejuni, C. lari, and C. coli in bird species capable of long-distance migration, many bird species could potentially act as vectors in long-distance transmission of these pathogens to domesticated animals or humans. For Salmonella spp., feeders have been regarded as likely sources for transmission of the bacteria between birds (31). This may also be the case for Campylobacter spp. Birds exposed to feed contaminated with Campylobacter spp. of human origin, or to feces contaminated with Campylobacter spp. of avian or human origin, could easily acquire infections. A recent study in which C. jejuni isolates from different sources were serotyped showed significant differences in serotype distribution between C. jejuni from wild birds and animals and from isolates of poultry or human origin, indicating that wildlife may be less important in the epidemiology of C. jejuni infections in humans (32). However, the number of wild-bird isolates included in the study was comparatively low. Given the diversity of habitats occupied by different bird species and the resulting possibility of different species being exposed to Campylobacter spp. from different sources, we feel that this question deserves further investigation.

The observed distribution of Campylobacter spp. in this study highlights the need for caution when considering wild birds as reservoirs. To correctly assess the impact of wild birds on Campylobacter epidemiology, it is essential to take into account the ecology of each bird species, i.e., its feeding habits, habitat preferences, migration patterns, life span, etc. Moreover, if prevalence changes along a temporal scale, that is, between different life stages like breeding, migration, molting, and wintering, comparisons of prevalence rates between studies can be misleading. Hence, it is of great importance to take ecological factors into consideration when investigating the potential role of wild birds as reservoirs and vectors of Campylobacter spp.

 
Many thanks to Paul Haemig for valuable comments on the manuscript.

This work was supported financially by the Health Research Council of Southeast Sweden (2001-2002), the Center for Environmental Research, the Medical Faculty of Umeå University, the Swedish Society of Medicine, and the Swedish Research Council for Environment, Agricultural Sciences, and Spatial Planning (FORMAS).

 
* Corresponding author. Mailing address: Department of Infectious Diseases, Umeå University, SE-901 87 Umeå, Sweden. Phone: 46 90 785 23 01. Fax: 46 90 13 30 06. E-mail: BjornOl{at}LTKALMAR.SE.

Contribution no. 178 from Ottenby Bird Observatory.

Top Abstract Introduction Materials and Methods Results Discussion References

 

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Applied and Environmental Microbiology, December 2002, p. 5911-5917, Vol. 68, No. 12
0099-2240/02/$04.00+0     DOI: 10.1128/AEM.68.12.5911-5917.2002
Copyright © 2002, American Society for Microbiology. All Rights Reserved.

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