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Article

Occurrence and Characteristics of Escherichia albertii in Wild Birds and Poultry Flocks in Switzerland

by
Karen Barmettler
1,
Michael Biggel
1,
Andrea Treier
1,
Francis Muchaamba
1,
Barbara Renate Vogler
2 and
Roger Stephan
1,*
1
Institute for Food Safety and Hygiene, Vetsuisse Faculty, University of Zurich, 8057 Zurich, Switzerland
2
National Reference Centre for Poultry and Rabbit Diseases (NRGK), Institute of Food Safety and Hygiene, Vetsuisse Faculty, University of Zurich, 8057 Zurich, Switzerland
*
Author to whom correspondence should be addressed.
Microorganisms 2022, 10(11), 2265; https://doi.org/10.3390/microorganisms10112265
Submission received: 19 October 2022 / Revised: 6 November 2022 / Accepted: 8 November 2022 / Published: 15 November 2022
(This article belongs to the Section Veterinary Microbiology)
Review Reports Versions Notes

Abstract

:
Escherichia albertii, a zoonotic pathogen, has sporadically been associated with infectious diarrhea in humans. Poultry and wild birds are considered potential reservoirs. We assessed the occurrence of E. albertii in 280 fecal samples from wild birds (n = 130) and pooled fecal samples collected at slaughterhouse level from poultry flocks (n = 150) in Switzerland. Using an E. albertii-specific PCR targeting the Eacdt gene, 23.8% (31/130) of the samples from wild birds, but not from the pooled poultry fecal samples, tested positive for Eacdt. The positive samples originated from 11 bird species belonging to eight families. Strain isolation was attempted on the PCR-positive samples by subculturing the broth cultures onto xylose–MacConkey plates. Isolation was possible on 12 of the 31 Eacdt-PCR-positive samples. Whole-genome sequencing revealed that the strains belonged to nine distinct sequence types, with ST13420 and ST5967 being represented by two and three isolates, respectively. All strains harbored the eae gene, while two strains were also positive for stx2f. Our study thus shows that E. albertii is present in the Swiss wild bird population, which can potentially act as a source of this pathogen to humans, other animals, and the environment.

1. Introduction

Escherichia albertii is a close relative of E. coli and has sporadically been associated with infectious diarrhea and foodborne outbreaks [1,2,3,4,5,6]. It was first described as an atypical eae-positive Hafnia alvei isolated in 1991 from a diarrheic child in Bangladesh [7], and was reclassified in 2003 as a new taxon in the genus Escherichia [8]. Due to its genetic and phenotypic similarity to other Enterobacteriaceae and the presence of eae, a virulence gene typically associated with enteropathogenic E. coli (EPEC) and enterohemorrhagic E. coli (EHEC), E. albertii is often misidentified in routine diagnostics [6,7,9,10,11,12,13,14,15,16].
In humans, clinical signs of E. albertii infection resemble those of a typical bacterial enteric infection, consisting of watery diarrhoea, nausea, vomiting, fever, abdominal pain, dehydration, and bloating [6,7,17]. Disease manifestations are linked to intestinal lesions and result from the combined action of intimin, an eae gene-encoded outer membrane protein, and type III secretion system effectors—similar to those caused by EHEC and EPEC [18,19,20]. Animals infected with E. albertii are often subclinically infected or die acutely with pathologic findings of septicaemia [18,21].
Some E. albertii strains have been reported to produce Shiga toxin 2a (Stx2a) or 2f (stx2f) [11,12,19,22,23]. Its clinical significance is not yet fully understood, but should not be underestimated, as Shiga toxin is the primary virulence factor of EHEC, and stx-positive E. albertii have sporadically been associated with bloody diarrhoea [24] and haemolytic uremic syndrome [25]. The virulence factor Stx2a is frequently associated with complicated infections and severe symptoms in humans, while stx2f has not yet been detected in severely ill patients. The clinical significance of stx2f-producing E. albertii is therefore still unknown [24,26]. Another important virulence factor is the cytolethal distending toxin (cdt). This toxin consists of three subunits (CdtA, CdtB, and CdtC) and is encoded in the Eacdt gene, which is highly specific for E. albertii [27]. The subunit CdtB acts as a DNAse and leads to DNA double-strand breaks, which in turn leads to irreversible cell cycle arrest [11]. The factor CDT has been associated with persistent colonization and invasion [28,29]. Wild-type E. albertii are susceptible to clinically relevant antibiotics, but the emergence of multi-drug-resistant clones has been reported [30].
A recently published up-to-date overview on the importance and occurrence of E. albertii is available [27]. In previous studies, birds have been described as potential carriers of E. albertii that might act as infection sources for humans [18,31,32,33]. Poultry were identified as a major source of multi-drug-resistant E. albertii in China [30]. In this study, we screened birds in Switzerland as potential carriers for E. albertii to assess the threat posed to people routinely handling these animals. Isolates were confirmed as E. albertii by Eacdt-specific PCR and further characterised by whole-genome sequencing.

2. Materials and Methods

2.1. Sample Collection

Fecal samples were collected between March and August 2022 from (1) avian patients at the rehabilitation center of the Swiss Ornithological Institute, (2) avian patients at the “Greifvogelstation Berg am Irchel”, (3) dead/injured birds collected by a gamekeeper of the city of Zurich, and (4) broiler flocks at a slaughterhouse. Overall, 280 samples were collected, representing 26 species from 13 orders (Table 1). Samples were taken by swabs (Transwab Amies sterile, with Amies medium MW170; HuberLab), using freshly defecated feces, or, in the case of dead birds, from the cloaca. For broilers, samples were taken at the slaughterhouse level from feces deposited in transport cages and pooled by flock. Samples from 150 flocks were collected, each consisting of 1921 to 17,513 birds (in total, 1,127,276 broilers). For all sampled wild birds, species, site of sample collection, date, age, sex, any clinical findings, cause of death, and as available, patient file number were recorded.

2.2. Bacterial Enrichement, Growth Conditions, and DNA Extraction

All swab samples were enriched in Enterobacteriaceae enrichment (EE) broth (Becton, Dickinson, Heidelberg, Germany) and incubated at 42 °C overnight. A loopful of each of the enrichment cultures was then plated on sheep blood agar (DifcoTM Columbia Blood Agar Base EH; Becton Dickinson AG, Allschwil, Switzerland), and again incubated at 42 °C overnight. The colonies were subsequently washed off with 2 mL 0.85% NaCl solution. Of this colony suspension, an aliquot (100 μL) was combined with 200 μL Gram-negative lysis buffer and heated at 60 °C for 50 min, followed by 99 °C for 10 min. After centrifugation (2 min; 11,000 rpm), the supernatant was used as template for the PCR.

2.3. Screening for the Eacdt Gene

All samples were tested for the presence of the cytolethal distending toxin (Eacdt) gene. The PCR was performed as previously described [34] with slight modifications, using GoTaq® Green Master Mix (Promega, Madison, WI, USA). The primer set EaCDTsp-F2 and EaCDTsp-R2 was used to specifically amplify a 449 bp fragment of the Eacdt gene. The E. albertii strain DSM 17528 was used as positive control, purified water as negative control. Amplification was done using the PCR thermocycler with cycle conditions of 5 min at 94 °C, followed by 30 cycles of 30 s at 94 °C, 30 s at 50 °C, 40 s at 72 °C, and lastly, 7 min at 72 °C. Results were analyzed using the Molecular Imager® Gel Doc™ XR System.

2.4. Isolation of E. albertii

In the event of an Eacdt-positive PCR result, one loopful of each of the respective colony suspensions was streaked onto xylose–MacConkey plates [35] and incubated at 42 °C overnight. Unlike E. coli, most E. albertii cannot ferment xylose, and colonies appear colorless to grey-white. These suspicious colonies were then confirmed as colonies of E. albertii by retesting them for the presence of Eacdt by the PCR described above. One positive colony per sample was stored in 25% glycerol at −80 °C for the strain collection bank.

2.5. DNA Extraction and Whole-Genome Sequencing (WGS)

For DNA extraction, the strains were grown on sheep blood agar at 42 °C overnight. DNA was isolated using the DNA Blood and Tissue Kit (Qiagen, Hombrechtikon, Switzerland), and DNA libraries were prepared using the Nextera DNA Flex Sample Preparation Kit (Illumina, San Diego, CA, USA). Whole-genome sequencing was performed using Illumina MiniSeq (Illumina, San Diego, CA, USA). Illumina read quality was assessed using FastQC 0.11.7 (Babraham Bioinformatics, Cambridge, UK), and genomes assembled with SPAdes 3.14.1 implemented in shovill 1.1.1 [36,37] using default settings. Multi-locus sequence types (STs) were determined using PubMLST (https://pubmlst.org/) and the Escherichia spp. Achtman scheme [38]. Acquired resistance genes were identified using AMRfinder 3.10.24 (default parameters) [39]. Virulence genes were identified using ABRicate 1.0.1 (https://github.com/tseemann/abricate) in combination with the Virulence Factor Database set B (sequence coverage 70%, identity 90%) [40]. The intimin encoding eae gene was typed using ABRicate 1.0.1 (sequence coverage 70%, identity 97%) in combination with the eae database provided by Luo et al. [30]. Subtypes of cdtB were identified using ABRicate 1.0.1 (sequence coverage 70%, identity 97%) with nucleotide sequences of accession numbers AAD10622 (cdtB-I), AAA18786 (cdtB-II), AAC45443 (cdtB-III/V), AAT92048 (cdtB-IV), and AST83_RS10865 (cdtB-VI) as references. E. albertii O and H antigen genotypes were determined by in silico PCR (https://github.com/egonozer/in_silico_pcr) in combination with primer pairs described by Ooka et al. [41] and Nakae et al. [42]. Only exact matches were considered. SNP distances were determined by read mapping using the CFSAN SNP Pipeline 2.2.1 for each ST cluster separately [43].

3. Results

Overall, 31 of 280 samples (11.1%) were PCR-positive for Eacdt (Table 1). The highest prevalence rates were found in yellow-legged gulls (Larus michahellis) (4/4, 100%) and carrion crows (Corvus corone) (15/24, 62.5%). Other positive samples originated from cormorant (Phalacrocorax carbo) (n = 1/1), magpie (Pica pica) (n = 2/5), red kite (Milvus milvus) (n = 1/3), sparrowhawk (Accipiter nisus) (n = 1/3), mallard (Anas platyrhynchos) (n = 1/4), white stork (Ciconia ciconia) (n = 1/4), brown owl (Strix aluca) (n = 1/7), common buzzard (Buteo buteo) (n = 3/23), and common kestrel (Falco tinnunculus) (n = 1/18). All poultry samples were PCR-negative.
By streaking colony suspensions onto xylose–MacConkey plates, E. albertii isolates could be recovered from 12 (38.7%) out of the 31 PCR-positive samples and were available for whole-genome sequencing. These originated from red kite (Milvus milvus) (n = 1/1), sparrowhawk (Accipiter nisus) (n = 1/1), magpie (Pica pica) (n = 1/2), yellow-legged gull (Larus michahellis) (n = 2/4), carrion crow (Corvus corone) (n = 6/15), and common buzzard (Buteo buteo) (n = 1/3) (Table 1).
Ribosomal MLST typing confirmed an E. albertii species affiliation for all 12 whole-genome sequenced isolates. They belonged to nine distinct sequence types, with ST13420 and ST5967 being represented by two and three isolates, respectively. The two ST13420 isolates differed by only one SNP and originated from carrion crows that were kept at the same rehabilitation facility. Similarly, two (KBV63i and KBV86i) of the three ST5967 isolates differed by one SNP, with the third isolate being more distantly related (~95 SNPs). KBV86i originated from a wild carrion crow, while KBV63i was obtained from an injured common buzzard at a rehabilitation facility.
All 12 isolates harbored eae genes, most of which were identical or near-identical to known variants (Table 2). The ST13420 isolates possessed a novel eae variant (96.0% sequence identity with eae alpha8). Two isolates (KBV38i and KBV70i) contained stx2f. All isolates harbored the cdtB subtype II, and the two stx2f-positive isolates additionally carried cdtB-I in a second copy of the cdtABC operon. In silico PCR assigned most isolates to one of five distinct O-antigen genotypes (EAOg4, EAOg12, EAOg16, EAOg32, and EAOg36). Three isolates carried putative novel variants. None of the 12 isolates harbored acquired antimicrobial resistance genes. All isolates harbored a chromosomal ampC gene encoding an intrinsic beta-lactamase.

4. Discussion

E. albertii is frequently found in birds. So far, E. albertii has been detected in birds in Scotland, North America, Australia, Japan, and Korea. It has been isolated from 29 species belonging to 22 families: Anatidae, Ardeidae, Artamidae, Cacatuidae, Columbidae, Corvidae, Falconidae, Fringillidae, Hirundinidae, Maluridae, Meliphagidae, Motacillidae, Passeridae, Phalacrocoracidae, Phasianidae, Picidae, Procellariidae, Psittacidae, Pycnonotidae, Rallidae, Rhipiduridae, and Sturnidae [18,21,32,33,44]. In this study, we examined a total of 280 fecal samples from 26 bird species for the presence of the Eacdt gene by PCR.
We were able to detect putative E. albertii in 11 species belonging to eight families: Accipitridae, Anatidae, Ciconiidae, Corvidae, Falconidae, Laridae, Phalacrocoracidae, and Strigidae. Four of the eleven species are waterbirds. Considering that E. albertii has been detected in environmental samples such as water [15,45,46], a transmission via water is conceivable and possibly involves other wild animals. Most of the other seven species, including birds of prey and corvidae, have in common that they mainly inhabit farmland and forests and that they feed on birds and/or small mammals. Considering that small mammals are often carriers of pathogens, it cannot be excluded that they might also be a reservoir for E. albertii. However, data on this hypothesis are so far lacking.
Previous studies found a variable prevalence of E. albertii in poultry, poultry meat, and giblets [1,13,30,47,48,49,50]. In this study, pooled fecal samples of 150 broiler flocks representing more than one million birds were investigated. We could not detect E. albertii in any of these samples, demonstrating that poultry is not a primary reservoir for E. albertii in Switzerland. Further investigations should focus on laying hens, as they are more often housed outdoors and may thus get infected through contact with wild birds.
Several studies have reported challenges in isolating E. albertii from PCR-positive samples [35,46,48,51]. Hinenoya et al. [52] reported a recovery rate of 25% in a study on the presence of E. albertii in raccoons. In addition, for stool from healthy humans, a detection limit of 105 CFU/g stool was reported [35]. In our study, the recovery rate was 38.7% (12/31). Other species such as Shigella boydii or Providencia stuartii are morphologically indistinguishable from E. albertii on the utilized selective medium, complicating the recovery of E. albertii [53]. Improved selective media are therefore needed to enable comprehensive epidemiological and clinical investigations of E. albertii. Alternatively, since we only considered colorless to grey-white colonies as suspicious, we might have missed lactose- or xylose-fermenting E. albertii, respectively, since these would not grow colorless [27]. Genome analyses of the 12 successfully recovered isolates identified two SNP clusters comprising two isolates each. One cluster was linked to carrion crows kept in the same rescue center, suggesting a recent transmission or acquisition from the same source, such as animal-to-animal spread or contaminated feed or water. The second cluster comprised isolates from a wild carrion crow and a buzzard from a bird sanctuary, pointing towards environmental transmission or indicating colonized prey as a potential source.
A sampling bias might exist for the wild birds since ill, injured, and dead birds were sampled. However, none of these birds showed clinical signs of intestinal infection, suggesting asymptomatic carriage. In conclusion, our study reveals that Escherichia albertii is present in the Swiss wild bird population, which can potentially act as a source of this pathogen to humans, other animals, and the environment.

Author Contributions

Conceptualization, K.B., A.T., B.R.V. and R.S.; methodology, K.B., A.T., F.M. and M.B.; formal analysis, K.B. and M.B.; investigation, K.B.; resources, R.S.; data curation, K.B. and M.B.; writing—original draft preparation, K.B.; writing—review and editing, R.S., M.B., B.R.V. and F.M.; supervision, R.S.; funding acquisition, R.S. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding.

Institutional Review Board Statement

This study was performed in accordance with the Swiss Animal Welfare Act (SR 455). No animals were killed for this study. No samples were taken directly from living animals. Therefore, no further ethical review and approval by the authority for animal experimentation is necessary for this study.

Informed Consent Statement

Not applicable.

Data Availability Statement

Sequencing read data and genome assemblies have been deposited at NCBI under BioProject accession number PRJNA879956.

Acknowledgments

The authors are grateful to Prisca Mattmann and team from the rehabilitation center of the Swiss Ornithological Institute in Sempach, Switzerland, Andi Lischke and team from the Greifvogelstation Berg am Irchel, Zurich, Switzerland, and Christian Breitler, Game keeper, City of Zurich, for the collaboration and sampling. Moreover, the authors would like to thank Nicole Cernela for her technical help in sequencing.

Conflicts of Interest

The authors declare no conflict of interest.

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Table
Table 1. List of sampled birds; number of Eacdt-positive samples and number of recovered E. albertii isolates.
Table 1. List of sampled birds; number of Eacdt-positive samples and number of recovered E. albertii isolates.
OrderFamilySpeciesNo. SpecimensNo. (%) Eacdt-PCR PositiveNo. E. albertii Isolates
AccipitriformesAccipitridaeBlack kite (Milvus migrans)300
Common buzzard (Buteo buteo)233 (13.0%)1
European honey buzzard (Pernis apivorus)100
Red kite (Milvus milvus)31 (33.3%)1
Sparrowhawk (Accipiter nisus)31 (33.3%)1
PandionidaeOsprey (Pandion haliaetus)100
AnseriformesAnatidaeMallard (Anas platyrhynchos)41 (25%)0
CharadriiformesLaridaeYellow-legged gull (Larus michahellis)44 (100%)2
CiconiiformesCiconiidaeWhite stork (Ciconia ciconia)41 (25%)0
ColumbiformesColumbidaeCommon wood pigeon (Columba palumbus)100
Feral pigeon (Columba livia domestica)1400
FalconiformesFalconidaeCommon kestrel (Falco tinnunculus)181 (5.6%)0
GalliformesPhasianidaeBroiler (Gallus gallus domesticus)15000
GruiformesRallidaeCoot (Fulica atra)100
PasseriformesTurdidaeBlackbird (Turdus merula)200
PasseridaeHouse sparrow (Passer domesticus)100
CorvidaeCarrion crow (Corvus corone)2415 (62.5%)6
Eurasian Jay (Garrulus glandarius)100
Magpie (Pica pica)52 (40%)1
Rook (Corvus frugilegus)200
PelecaniformesArdeidaeGray heron (Ardea cinerea)100
PodicipediformesPodicipedidaeGreat crested grebe (Podiceps cristatus)300
StrigiformesStrigidaeBrown owl (Strix aluco)71 (14.3%)0
Eagle owl (Bubo bubo)200
Long-eared owl (Asio otus)100
SuliformesPhalacrocoracidaeCormorant (Phalacrocorax carbo)11 (100%)0
Total 28031 (11.1%)12
Table
Table 2. Sequence types and presence of stx, eae subtype, cdtB subtype, and O- and H-antigen subtypes in E. albertii genome assemblies.
Table 2. Sequence types and presence of stx, eae subtype, cdtB subtype, and O- and H-antigen subtypes in E. albertii genome assemblies.
IsolateSourceFacilityMLSTstx Subtypeeae Subtype (Sequence Identity) * cdtB SubtypeO-Antigen GenotypeH-Antigen GenotypeAccession Number
KBV4iCarrion crowRSOIST13420-NovelcdtB-IIEAOg36EAHg1GCA_025600035.1
KBV24iCarrion crowRSOIST13420-NovelcdtB-IIEAOg36EAHg1GCA_025599995.1
KBV30iCarrion crowRSOIST5967-sigma2 (99.9%)cdtB-IIEAOg36EAHg2GCA_025599955.1
KBV26iMagpieRSOIST5399-sigma2 (99.96%)cdtB-IIEAOg32EAHg2GCA_025599965.1
KBV27iCarrion crowRSOIST4685-alpha9 (100%)cdtB-IIEAOg12EAHg1GCA_025599935.1
KBV38iYellow-legged gullRSOIST8692stx2fxi (99.97%)cdtB-I, cdtB-IINovelEAHg3GCA_025599905.1
KBV42iCarrion crowRSOIST7834-not determined (incompletely assembled)cdtB-IINovelEAHg1GCA_025599895.1
KBV63iCommon buzzardGBIST5967-sigma2 (99.9%)cdtB-IIEAOg36EAHg2GCA_025599875.1
KBV70iSparrowhawkGBIST11471stx2fsigma (100%)cdtB-I, cdtB-IIEAOg4EAHg4GCA_025599835.1
KBV72iRed kiteGBIST4170-alpha8 (100%)cdtB-IIEAOg16EAHg1GCA_025599845.1
KBV86iCarrion crowEST5967-sigma2 (99.9%)cdtB-IIEAOg36EAHg2GCA_025599815.1
KBV115iYellow-legged gullEST3296-lambda2 (100%)cdtB-IINovelEAHg4GCA_025599765.1
* According Luo et al. [30]; ≥97% sequence identity, 100% sequence coverage. RSOI: Rehabilitation Center of the Swiss Ornithological Institute; GBI: Greifvogelstation Berg am Irchel; E: environment.
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Barmettler, K.; Biggel, M.; Treier, A.; Muchaamba, F.; Vogler, B.R.; Stephan, R. Occurrence and Characteristics of Escherichia albertii in Wild Birds and Poultry Flocks in Switzerland. Microorganisms 2022, 10, 2265. https://doi.org/10.3390/microorganisms10112265

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Barmettler K, Biggel M, Treier A, Muchaamba F, Vogler BR, Stephan R. Occurrence and Characteristics of Escherichia albertii in Wild Birds and Poultry Flocks in Switzerland. Microorganisms. 2022; 10(11):2265. https://doi.org/10.3390/microorganisms10112265

Chicago/Turabian Style

Barmettler, Karen, Michael Biggel, Andrea Treier, Francis Muchaamba, Barbara Renate Vogler, and Roger Stephan. 2022. "Occurrence and Characteristics of Escherichia albertii in Wild Birds and Poultry Flocks in Switzerland" Microorganisms 10, no. 11: 2265. https://doi.org/10.3390/microorganisms10112265

APA Style

Barmettler, K., Biggel, M., Treier, A., Muchaamba, F., Vogler, B. R., & Stephan, R. (2022). Occurrence and Characteristics of Escherichia albertii in Wild Birds and Poultry Flocks in Switzerland. Microorganisms, 10(11), 2265. https://doi.org/10.3390/microorganisms10112265

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