Wild, insectivorous bats might be carriers of Campylobacter spp.


previous item | next item

Citation
Wild, insectivorous bats might be carriers of Campylobacter spp.

Material Information

Title:
Wild, insectivorous bats might be carriers of Campylobacter spp.
Series Title:
PLOS ONE
Creator:
Hazeleger , Wilma C.
Jacobs-Reitsma, Wilma F.
Lina, Peter H. C.
de Boer, Albert G.
Bosch, Thijs
Hoek, Angela H. A. M. van
Beumer, Rijkelt R.
Publisher:
PLOS
Publication Date:
Physical Description:
1 online resource

Subjects

Subjects / Keywords:
Campylobacter ( lcsh )
Bats -- Pathogens ( lcsh )
Genre:
serial ( sobekcm )
Location:
Europe -- Netherlands

Notes

Abstract:
The transmission cycles of the foodborne pathogens Campylobacter and Salmonella are not fully elucidated. Knowledge of these cycles may help reduce the transmission of these pathogens to humans. The presence of campylobacters and salmonellas was examined in 631 fresh fecal samples of wild insectivorous bats using a specially developed method for the simultaneous isolation of low numbers of these pathogens in small-sized fecal samples (≤ 0.1 g). Salmonella was not detected in the feces samples, but thermotolerant campylobacters were confirmed in 3% (n = 17) of the bats examined and these pathogens were found in six different bat species, at different sites, in different ecosystems during the whole flying season of bats. Molecular typing of the 17 isolated strains indicated C. jejuni (n = 9), C. coli (n = 7) and C. lari (n = 1), including genotypes also found in humans, wildlife, environmental samples and poultry. Six strains showed unique sequence types. This study shows that insectivorous bats are not only carriers of viral pathogens, but they can also be relevant for the transmission of bacterial pathogens. Bats should be considered as carriers and potential transmitters of Campylobacter and, where possible, contact between bats (bat feces) and food or feed should be avoided.

Record Information

Source Institution:
University of South Florida
Holding Location:
University of South Florida
Rights Management:
All applicable rights reserved by the source institution and holding location.
Resource Identifier:
K26-05440 ( USFLDC DOI )
k26.5440 ( USFLDC Handle )

USFLDC Membership

Aggregations:
University of South Florida
Karst Information Portal

Postcard Information

Format:
serial

Downloads

This item is only available as the following downloads:


Full Text

PAGE 1

RESEA RCH ARTICL E Wild, insectivorous bats might be carriers of Campylobacter spp. Wilma C. Hazeleger 1 r, Wilma F. Jacobs-Reitsma 2^ , Peter H. C. Lina 3 , Albert G. de Boer 4 , Thijs Bosch 5 , Angela H. A. M. van Hoek 6 , Rijkelt R. Beumer 1 1 Laboratory of Food Microbiol ogy, Wageni ngen University & Researc h, Wageningen, Netherlands , 2 RIKILT Institute of Food Safety, Wageningen, Netherlan ds, 3 Naturalis Biodive rsity Center, Leiden, Netherlan ds, 4 Wageni ngen Bioveterinar y Research, Wagenin gen University & Research, Lelystad, Netherlan ds, 5 Ad Hoc Ecotechni ek, Arnhem, Netherlan ds, 6 RIVM National Institute for Public Health and the Enviro nment, Bilthove n, Netherlan ds ^ Current address: RIVM National Institute for Public Health and the Environ ment, Bilthove n, Netherlan ds Wilma.H azeleger@ wur.nl Abstract Background The transmission cycles of the foodborne pathogens Campylobacter and Salmonella are not fully elucidated. Knowledge of these cycles may help reduce the transmission of these pathogens to humans. Methodology/principal findings The presence of campylobacters and salmonellas was examined in 631 fresh fecal samples of wild insectivorous bats using a specially developed method for the simultaneous isolation of low numbers of these pathogens in small-sized fecal samples ( 0.1 g). Salmonella was not detected in the feces samples, but thermotolerant campylobacters were confirmed in 3% (n = 17) of the bats examined and these pathogens were found in six different bat species, at different sites, in different ecosystems during the whole flying season of bats. Molecular typing of the 17 isolated strains indicated C. jejuni (n = 9), C. coli (n = 7) and C. lari (n = 1), including genotypes also found in humans, wildlife, environmental samples and poultry. Six strains showed unique sequence types. Conclusion/significance This study shows that insectivorous bats are not only carriers of viral pathogens, but they can also be relevant for the transmission of bacterial pathogens. Bats should be considered as carriers and potential transmitters of Campylobacter and, where possible, contact between bats (bat feces) and food or feed should be avoided. Introduction n and r are the two most important zoonotic bacteria in Europe [1], and these pathogens are commonly transmitted to humans via food, often of animal origin. PLOS ONE | https://doi.or g/10.137 1/journal.po ne.01906 47 January 11, 2018 1 / 10 a1111111111 a1111111111 a1111111111 a1111111111 a1111111111 23(1 $&&(66 Citation: Hazelege r WC, Jacobs-Re itsma WF, Lina PHC, de Boer AG, Bosch T, van Hoek AHAM, et al. (2018) Wild, insectivor ous bats might be carriers of Campyloba cter spp.. PLoS ONE 13(1): e0190647. https://d oi.org/10.1371/j ournal. pone.019064 7 Editor: Michelle L. Baker, CSIRO, AUSTRALIA Received: April 20, 2017 Accepted: December 18, 2017 Published: January 11, 2018 Copyright: ‹ 2018 Hazelege r et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricte d use, distribu tion, and reproduction in any medium, provided the original author and source are credited. Data Availabilit y Statement: All relevant data are within the paper and its supporting files. The typing information is uploaded to: https:// pubmlst.org / campylob acter/. Funding: Ad Hoc provided support in the form of salaries for author TB, but did not have any additional role in the study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing interests : Ad Hoc provided support in the form of salaries for author TB, but did not have any additiona l role in the study design, data

PAGE 2

Since the transmission cycles of both bacteria are not fully revealed, it is useful to search for possible reservoirs in the environment since different species of wildlife, such as wild birds, are known to be potential carriers of n [2±4] and r [5]. So far, bats are identified to be potential carriers of mainly viral pathogens [6, 7] but they might also be relevant in the transmission cycles of n and r. Thus far, information on the presence of n in bats is rare [8] or only suspected [9], but other bacterial pathogens have been isolated occasionally from bats around the world, such as r and r [10]. In Western Europe, all bat species are insectivorous (Microchiroptera). The fact that insects are able to transmit n [11±13] or r [14] for instance via feces of farm animals or water birds, leads to the assumption that they might be a source of infection for bats as well. By contaminating water, crops, fruit, feed or soil with their feces, it could be speculated that infected bats might in turn play a part in the transmission of these bacteria. An opportunity arose to participate in an ongoing surveillance on viruses in bats. In this investigation fresh fecal samples of wild bats were examined for the presence of n and r . For epidemiological purposes, 17 isolated n strains were typed using real-time PCR, matrix-assisted laser desorption and ionization-time-of-flight mass spectrometry (MALDI-TOF MS) and multilocus sequence typing (MLST) was performed by Sanger sequencing and/or whole genome sequencing (WGS). Material and methods Ethical statement All procedures were carried out in strict compliance with the Flora and Fauna Act licenses FF/ 75A/2003/150 and FF/75A/2003/169/a/b, issued by the former Dutch Ministry of Agriculture, Nature and Food Quality, and with permission of all site owners (Staatsbosbeheer; Limburgs Landschap). All bats were released within one hour at the point of capture. Bacterial strains n C356 and r Livingstone (both from the culture collection of the RIVM, Bilthoven, Netherlands) were cultured in Brain Heart Infusion broth (BHI, Becton Dickinson and Company, Sparks, USA) for use as positive controls. n cultures were grown for two days at 41.5ÊC in micro-aerobic atmosphere achieved by flushing jars with the appropriate gas mixture (10% CO 2 , 5% O 2 and 85% N 2 ) and r was cultured for 24 h at 37ÊC, unless stated otherwise. All strains were maintained as overnight cultures in BHI with 15% glycerol at -80ÊC. Bat feces sampling Active surveillance programs examining bats for the presence of several viruses such as rabies provided fecal samples from 631 bats for this study. In 2007 and 2008, bats were caught during the flying season (April-October) in several regions of the Netherlands (Fig 1). With exception of a few grounded bats, bats were caught with mist-nets in their foraging habitats in forests or over water bodies, and in the southernmost part of the country in the province of Limburg at swarming sites at the entrances of limestone mines [15]. After catching, each bat was kept (not sedated) in a sterile cotton bag for about 30 min for the collection of fecal pellets after which, if possible, the species, sex, age and reproductive status were determined. All bats were released at their capture site. Fecal samples were taken with swabs (Transystem Amies medium transport swabs; 108.USE, Copan Diagnostics Inc, Murietta, USA) either from the cotton bag or directly from the animals if defecation occurred during handling of the bats. Swab samples Campyl obacter ssp. in bats PLOS ONE | https://doi.or g/10.137 1/journal.po ne.01906 47 January 11, 2018 2 / 10 collection and analysis , decision to publish, or preparation of the manuscript. The authors confirm that the affiliation with Ad Hoc does not alter their adherence to all PLOS ONE policies on sharing data and materials and no competing interests exist. The authors have no restrictio ns on sharing data and/or materials.

PAGE 3

were kept in transport medium at 0±4ÊC for a maximum of two days before microbiological examination was started. Isolation of and nr A method was developed for simultaneous isolation of low numbers of r and n both from one small-sized fecal sample ( 0.1 g). In a pre-trial, using all components in the transport swabs and -media, it was possible to easily recover both pathogens from fecal samples after two to seven days of storage of the swabs (at 0±4ÊC) at levels as low as 10± 100 CFU per swab [16]. Methods and media described in the ISO-protocols for r [17] and n [18] were adapted as follows: for direct isolation of n, the swabs containing fecal material were streaked onto modified charcoal cefoperazone deoxycholate agar (mCCDA) plates and subsequently put in 10 ml buffered peptone water (BPW). The transport medium of the transport tube was mixed with 5 ml of Bolton Broth (BB) and incubated for 4 h at 37ÊC, and subsequently for 44 h at 41.5ÊC in micro-aerobic atmosphere (see above). After mixing the BPW suspension plus swab, one ml was transferred to 9 ml of Preston Broth (PB) for selective enrichment of n, since this medium has shown to give better selectivity compared to BB [19, 20]. The contents of PBand BB-tubes were streaked onto mCCDA after 24 and 48 h of incubation at 41.5ÊC in micro-aerobic conditions. The mCCDA plates were incubated under micro-aerobic conditions for 48 h at 41.5ÊC. Suspect colonies were confirmed by microscopy and a latex agglutination test for n (M46CE, Microgen Bioproducts, Camberley UK). For detection of r, the remainder of the BPW was incubated at 37ÊC for 16±20 h after which three drops of BPW were spotted onto the center of a modified semi-solid rappaport vassiliadis (MSRV) plate (incubated at 41.5ÊC for 24 and 48 h). Suspect growth was then streaked onto brilliant green agar/xylose Fig 1. Catching sites of n r-pos itive bats in the Netherlands. https://d oi.org/10.1371/j ournal.pon e.0190647.g0 01 Campyl obacter ssp. in bats PLOS ONE | https://doi.or g/10.137 1/journal.po ne.01906 47 January 11, 2018 3 / 10

PAGE 4

desoxycholate agar plates (BGA/XLD) which were incubated for 24 h at 37ÊC. Suspect colonies from BGA/XLD were streaked to neutral medium (Nutrient agar) and further confirmed for r using Wellcolex Colour Salmonella (Remel Europe, Dartford, UK). All media except BHI were purchased from Oxoid, Basingstoke, UK. Typing of nr strains The isolated strains were initially tested using duplex real-time PCR as described previously [21] to determine . and . . Furthermore, MALDI-TOF MS analyses were performed to obtain further information on the remaining unidentified strains with a Bruker Daltonics MALDI Biotyper [22] using a database collection of strains as mentioned in S1 Table. Multilocus sequence typing (MLST) was done by Sanger sequencing using loci , , n, , , and nn [23, 24]. Instant, multilocus batch query (https://pubmlst.org/ campylobacter/) [25] was done by using the MLST plugin from Bionumerics 6.1 (Applied Maths, Austin, USA). The seventeen strains were then subjected to whole genome sequence (WGS) analysis. Strains were grown micro-aerobically in 10 ml Heart Infusion broth (bioTRADING, Mijdrecht, the Netherlands) with gentle shaking at 37ÊC for 24 h. Cell pellets were obtained by centrifugation, they were washed and dissolved in 200 l DNA/RNA Shield (Zymo Research, Irvine, CA, USA). DNA isolation, fragmentation and library preparation for whole genome sequencing was outsourced to an independent service company (BaseClear, Leiden, the Netherlands). The isolates were sequenced on a HiSeq 2500 sequencer (BaseClear, Leiden, the Netherlands). assembly of the WGS data was performed using Velvet [26]. basic local alignment search tool (BLAST) analysis with the sequences of universal n primers and probes [27] against the assembled genomes was performed to confirm the genus. Additionally, BLAST analysis with sequences of probes specific for . , . , . and . [28] was performed to determine the n species . MLST was performed on the assemblies via the public n MLST database (https://pubmlst.org/campylob acter/). Results and discussion Detection of nr and nconfirmed strains were found in 17 out of 631 fecal samples (3%; Table 1), in six out of 14 different bat species from diverse habitats (Fig 1 and Table 2) throughout the flying season. These findings are in accordance with the study of Hatta et al. [29], who found partial genomes of . and . in rectal swab samples of fruit bats. However, Adesiyun et al. [30] tested gastrointestinal tracts of 377 bats in Trinidad and Tobago and did not find any campylobacters. This could be explained by climate differences or by the fact that rather than with enrichment broths, the study was carried out using selective plates, which do not easily allow growth of sub-lethally damaged cells. A quantitative metagenomic analysis of bat fecal bacteria in Finland did not show any genomic DNA of n, but in this case, only one Daubenton's Bat (n n) was examined [31]. From the fecal samples of the bats, multiple routes were followed to maximize the chance of n isolation; direct streak on mCCDA, or after enrichment in BB and PB. From two n-positi ve samples, bacterial strains were isolated via all routes (S2 Table). However, in 9 out of the 17 samples (53%), the bacterium was only isolated via the PB route. In most of those cases, the plates from the BB enrichment were overgrown with contaminating flora, preventing recognition and isolation of n colonies. This confirms other findings of PB being more selective than BB in the detection of n [19, 20, 32]. Campyl obacter ssp. in bats PLOS ONE | https://doi.or g/10.137 1/journal.po ne.01906 47 January 11, 2018 4 / 10

PAGE 5

This study was biased with respect to catching sites due to dependency on ongoing research, which was mainly focusing on bats in the middle and southern part of the Netherlands. No correlation could be found between gender of the bats and n carriage. Except for Table 1. Number of nr positive bats (total number of bats sampled) in 2007 and 2008. Bat species 2007 2008 n n ns a 0 (29) n n ns 2 (28) n n ns 0 (11) n 2 (25) 0 (13) n n 0 (15) 8 (164) n n ns 1 (70) n n ns 0 (6) n n ns 0 (20) n nn ns 0 (27) n n 2 (11) 0 (2) n n 0 (5) 0 (4) n n 0 (6) 2 (96) n n 0 (2) 0 (24) n n ns 0 (2) Microch iroptera, not further specified ns 0 (71) a ns: not sampled https://d oi.org/10.1371/j ournal.pon e.0190647.t00 1 Table 2. Information of isolated strains: Catching date and -location of the bats, bat species, nr species, Sequence Type (ST) and clonal complex (if existing). Strain Date Location a Bat species n r species c ST Clonal complex 1 04-18-0 7 Stompwijk (ZH) n 991 ST-692 2 06-08-0 7 Noordwijke rhout (ZH) n n 432 ST-61 3 06-08-0 7 Noordwijke rhout (ZH) n n 583 ST-45 4 06-19-0 7 Ter Aar (ZH) n 704 5 07-04-0 8 Gastel (NB) n n 334 ST-45 6 07-15-0 8 Arnhem/Nijmeg en area (GLD) n n 2007 7 07-15-0 8 Arnhem/Nijmeg en area (GLD) n n 2007 8 07-15-0 8 Arnhem/Nijmeg en area (GLD) n n 9007 d 9 07-15-0 8 Arnhem/Nijmeg en area (GLD) n n 8159 d 10 08-04-0 8 Schark b (L) n n 19 ST-21 11 08-18-0 8 Schenk b (L) n n 7255 d 12 08-25-0 8 Barakken b (L) n n 138 d 13 08-25-0 8 Koelenbosc h b (L) n n 9005 d 14 09-01-0 8 Boschberg b (L) n n 267 ST-283 15 09-08-0 8 Boschberg b (L) n n 9006 d 16 09-15-0 8 Sibbergroev e b (L) n n 48 ST-48 17 09-22-0 8 Boschberg b (L) n n 2274 a ZH = province of Southern Holland; NB = province of Northern Brabant; GLD = province of Gelderla nd; L = province of Limburg b Limestone mine c For technical details about species identificat ion and typing is referred to S3 Table d New MLST registered https://do i.org/10.1371/j ournal.pone .0190647.t002 Campyl obacter ssp. in bats PLOS ONE | https://doi.or g/10.137 1/journal.po ne.01906 47 January 11, 2018 5 / 10

PAGE 6

the two n-positive Noctule Bats (n n) that had diarrhea, bats generally looked healthy with solid droppings, indicating that most bats are probably healthy carriers. r was not isolated from any of the samples in the present study. Since the aim was to determine the presence of both n and r, splitting-up the material and the small sample quantity (<10±100 mg) could lead to an underestimation of the number of positive animals and this could also explain the fact that r was not found. Furthermore, it has been reported that r shedding in animals like chickens [13] and pigs [33] can be intermittent; this could also be the case in bats. Other studies did mention presence of r in vespertilionid bats, for instance in 0.6% of 486 carcasses of deceased animals in Germany [34] or in 2% of 96 live bats in the Philippines, but in the latter case, r could not be cultured and was found only with PCR techniques [35]. r spp. have also been occasionally isolated from other bat families [30,36,37]. Genetic characterization . was the most common species found (9 times; Table 2). Identification to the species level proved to be difficult for seven strains. Six strains were negative in the real-time PCR for . or . but using MALDI-TOF MS, these strains were designated as probably n, with unreliable . indication (Table 2, S3 Table). One strain (strain 12) could not be further identified with either of these techniques. Fortunately, WGS data analysis did allow speciation of all strains. basic local alignment search tool (BLAST) analysis with the sequences of universal n primers and probes [27] against the assembled genome of strain 12 showed 100% matches, confirming that it was a n (data not shown). Additionally, BLAST analysis with sequences of probes specific for . , . , . and . [28], revealed the highest match of 87% with . (Table 2 and S3 Table). Because of this relatively low similarity, strain 12 was also typed with the SpeciesFinder 1.2 service at the Center for Genomic Epidemiology website (https://cge.cbs.dtu.dk/services/Spe ciesFinder/). The outcome was again . (data not shown). For six isolates new alleles and STs were assigned by the curators of the and nonMLST databases (S3 Table). MLST results indicated that n strains isolated from bats were similar to the types previously found in various sources such as humans, environmental waters, food, poultry and other animals (Table 3 and S3 Table; [27]). The sources of infection for bats are most probably other bats in the same colony, contaminated water or insects that were in contact with contaminated water or animal feces. A total of 16 different sequence types (ST) were identified (Table 2) of which seven belonged to a clonal complex. The six different clonal complexes identified were ST-21, ST-45, ST-48, ST-61, ST-283 and ST-692 (Tables 2 and 3). Two strains within the clonal complex ST-45 were found on different dates at different locations in different bat species. Clonal complexes ST-45 and ST-61 are among the most frequently isolated genotypes in humans [38] and are also found in other studies in wildlife and water samples [39]. Six new STs were identified in six strains (Table 2 and S3 Table). All isolates of one bat, obtained from the different isolation methods resulted in the same MLST types. The feces samples from both Noctule Bats, sampled at the same spot and day, were positive for n. However STs and clonal complexes (strains 2 and 3 in Table 2) were different, demonstrating that within local populations different n types exist. Conclusions In conclusion, despite the drawbacks of the methods, n was found in fecal samples of six different bat species, at different sites, in different ecosystems during the whole Campyl obacter ssp. in bats PLOS ONE | https://doi.or g/10.137 1/journal.po ne.01906 47 January 11, 2018 6 / 10

PAGE 7

flying season of bats. Molecular typing of the strains indicated genotypes also found in humans, wildlife, environmental samples and poultry. Therefore, bats could be considered as possible carriers and transmitters of n like birds and rodents. Where possible, contact between bats (bat feces) and food or feed should be avoided. Supporting information S1 Table. Relevant strains present in MALDI TOF MS database used for typing of the nr strains. (XLSX) S2 Table. Isolation routes of nr from bat fecal samples. mCCDA: direct isolation on mCCDA plates; BB 24 h and BB 48 h: isolation via enrichment procedure in Bolton Broth incubated for 24 h and 48 h respectively; PB 24 h and PB 48 h: isolation via enrichment procedure in Preston Broth incubated for 24 h and 48 h respectively. (DOCX) S3 Table. Combined confirmationand typing data of 17 nr strains isolated from bats. The following techniques were used: duplex real-time PCR for determination of . and . ; Multilocus Sequence typing (resulting in Sequence Types (ST)); MALDI TOF MS (Maldi); Whole Genome sequencing (WGS); Sequence Typing ( ST). For strains 8, 16 and 17, multiple isolates were typed. (XLSX) Acknowledgmen ts The authors thank Anne-Jifke Haarsma, Johannes Regelink, Jasja Dekker, Jaap van Schaik, and Rene  Janssen for collecting fecal samples in the midst of catching and describing bats for their own research. Anne-Jifke Haarsma is acknowledged for drawing Fig 1, Wendy van Overbeek for excellent technical assistance and Marcel van Bergen for support with n typing. Table 3. Clonal complexes of n r sequence types found in feces from bats and common sources of isolates within the MLST database (https://pubm lst.org/cam pylobacter /). Strain Clonal complex Number of STs in clonal complex a Common sources 1 ST-692 75 Cattle, environment al waters, human, poultry, wild bird 2 ST-61 178 Cattle, environment al waters, farm environmen t, human, other animal, poultry, sheep 3 ST-45 345 Cat, cattle, dog, environme ntal waters, farm environ ment, human, other animal, other food, poultry, sheep, wild bird 5 ST-45 345 Cat, cattle, dog, environme ntal waters, farm environ ment, human, other animal, other food, poultry, sheep, wild bird 10 ST-21 753 Cattle, dog, environment al waters, farm environmen t, human, other animal, other food, pig, poultry, sheep, turkey, wild bird 14 ST-283 56 Cattle, dog, environment al waters, human, other animal, other food, potable/drink ing water, poultry, sheep, wild bird 16 ST-48 220 Cattle, dog, environment al waters, farm environmen t, human, other animal, other food, pig, poultry, sand (bathing beach), sheep a As of Sep. 15 th 2017 https://d oi.org/10.1371/j ournal.pon e.0190647.t00 3 Campyl obacter ssp. in bats PLOS ONE | https://doi.or g/10.137 1/journal.po ne.01906 47 January 11, 2018 7 / 10

PAGE 8

This publication made use of the n Multi Locus Sequence Typing website (https://pubmlst.org/campylob acter/) sited at the University of Oxford. The development of this site has been funded by The Wellcome Trust. Author Contributions Conceptualization: Wilma C. Hazeleger, Wilma F. Jacobs-Reitsma, Peter H. C. Lina, Rijkelt R. Beumer. Data curation: Wilma C. Hazeleger, Wilma F. Jacobs-Reitsma, Peter H. C. Lina, Rijkelt R. Beumer. Formal analysis: Wilma C. Hazeleger, Wilma F. Jacobs-Reitsma, Peter H. C. Lina, Albert G. de Boer, Thijs Bosch, Angela H. A. M. van Hoek, Rijkelt R. Beumer. Investigation: Wilma C. Hazeleger, Wilma F. Jacobs-Reitsma, Peter H. C. Lina, Albert G. de Boer, Thijs Bosch, Angela H. A. M. van Hoek, Rijkelt R. Beumer. Methodology: Wilma C. Hazeleger, Wilma F. Jacobs-Reitsma, Peter H. C. Lina, Albert G. de Boer, Thijs Bosch, Angela H. A. M. van Hoek, Rijkelt R. Beumer. Project administration: Wilma C. Hazeleger. Supervision: Wilma C. Hazeleger. Writing ± original draft: Wilma C. Hazeleger, Wilma F. Jacobs-Reitsma, Peter H. C. Lina, Albert G. de Boer, Thijs Bosch, Rijkelt R. Beumer. Writing ± review & editing: Wilma C. Hazeleger, Wilma F. Jacobs-Reitsma, Peter H. C. Lina, Albert G. de Boer, Angela H. A. M. van Hoek, Rijkelt R. Beumer. References 1. European Food Safety Authority and European Centre for Disease Preven tion and Control. The European Union summary report on trends and sources of zoonoses, zoonotic agents and food-borne outbreaks in 2014. EFSA J. 2015; 13: 4329, 191 pp. https:// doi.org/10.29 03/j.efsa.20 15.4329 2. Sippy R, Sandova l-Green CMJ, Sahin O, Plummer P, Fairbank s WS, Zhang Q, et al. Occurrenc e and molecular analysis of Campyloba cter in wildlife on livestoc k farms. Vet Microbiol . 2012; 157: 369±375. https://doi.or g/10.101 6/j.vetmic. 2011.12.026 PMID: 222661 57 3. Brown PE, Christens en OF, Clough HE, Diggle PJ, Hart CA, Hazel S, et al. Frequency and spatial distribution of environ mental Campyl obacter spp. Appl Environ Microbiol . 2004; 70: 6501±6511. https://doi. org/10.1128/ AEM.70.11. 6501-6511.2 004 PMID: 155285 12 4. Wahlstro È m H, Tyse  n E, Engvall EO, Bra È ndstrom B, Eriksson E, Mo È rner T, et al. Survey of Campyl obacter species, VTEC O157 and Salmonella species in Swedish wildlife. Vet Rec, J British Vet Ass. 2003; 153: 74±80. 5. Hilbert F, Smulders FJM, Chopra-De wasthaly R, Paulsen P. Salmon ella in the wildlife-hum an interface . Food Res Intern. 2012; 45: 603±8. 6. Clayton BA, Wang LF, Marsh GA. Henipavirus es: an updated review focusing on the pteropid reservoir and features of transmission. Zoon Public Health. 2013; 60: 69±83. https://doi.or g/10.111 1/j.18632378.2012. 01501.x PMID: 22709528 7. Ng JHJ, Baker ML. Bats and bat-bo rne diseases : a perspective on Australian megabats. Austral J Zool. 2013; 61: 48±57. http://dx.doi.o rg/10.1 071/ZO12126 . 8. Child J. Bats in my belfry. Lancet. 1994; 343: 5±6. PMID: 790505 6 9. Palmer SR, Gully PR, White JM, Pearson AD, Suckling WG, Jones DM, et al. Water-born e outbreak of Campylo bacter gastroent eritis. Lancet. 1983; 321: 287±29 0. 10. Mu È hldorfer K. Bats and Bacterial Pathogen s: A Review. Zoon Public Health. 2013; 60: 93±103. 11. Szalanski AL, Owens CB, McKay T, Steelman CD. Detection of Camp ylobacter and Escherichia coli O157:H7 from filth flies by polymera se chain reaction. Med Vet Entom. 2004; 18: 241±6. Campyl obacter ssp. in bats PLOS ONE | https://doi.or g/10.137 1/journal.po ne.01906 47 January 11, 2018 8 / 10

PAGE 9

12. Hald B, Skovgnrd H, Bang DD, Peders en K, Dybdahl J, Jespersen JB, et al. Flies and Camp ylobacter infection of broiler flocks. Emerg Infect Dis. 2004; 10: 1490±2 . https://doi.or g/10.3201 /eid1008.0401 29 PMID: 154962 57 13. Hazeleger WC, Bolder NM, Beumer RR, Jacobs-Reits ma WF. Darkling beetles (Alphitobiu s diaperinus) and their larvae as potential vectors for the transfer of Campylobac ter jejuni and Salmonella enterica serovar Paratyp hi B variant Java between successive broiler flocks. Appl Environ Microbiol . 2008; 74: 6887±6891. https:/ /doi.org/10.11 28/AEM .00451-08 PMID: 187910 34 14. Mian LS, Maag H, Tacal JV. Isolation of Salmonella from muscoid flies at comme rcial animal establishments in San Bernardin o County, Californi a. J Vector Ecol. 2002; 27: 82±5. PMID: 12125877 15. Van Schaik J, Janssen R, Bosch T, Haarsma A-J, Dekker JJA, Kranstauber B. Bats swarm where they hibernate: compos itional similarity between autumn swarmi ng and winter hibernation assemb lages at five undergrou nd sites. PLoS ONE. 2015; 10(7): e0130850. https:// doi.org/10.13 71/journal.p one. 0130850 PMID: 26153691 16. Hazeleger WC, Beumer RR. Survival of Campyl obacter and Salmon ella in transport medium. In: Abstract book 15th International Workshop on Campyl obacter, Helicobac ter and related organisms CHRO20 09, Niigata, Japan, abstr O9-1. 2009: p 66. 17. International Organizat ion for Standardizati on. ISO 6579:20 02: Microbiology of food and animal feeding stuffsÐHo rizontal method for detection of Salmonella spp. International Organizatio n for Standa rdization, Geneva , Switzerlan d; 2002. 18. International Organizat ion for Standardizati on. ISO 10272±1: 2006: Microbiol ogy of food and animal feeding stuffsÐ Horizontal method for detection and enumer ation of Campylobac ter spp.±Part1: Detection method. International Organizat ion for Standardizati on, Geneva , Switzerlan d; 2006. 19. Jasson V, Samper s I, Botteldo orn N, Lo  pez-Ga  lvez F, Baert L, Denay er S, et al. Character ization of Escherich ia coli from raw poultry in Belgium and impact on the detection of Campyloba cter jejuni using Bolton Broth. Int J Food Microbiol . 2009; 135: 248±25 3. https://doi.or g/10.101 6/j.ijfoodmic ro.2009.09. 007 PMID: 197863 12 20. Habib I, Uyttendaele M, de Zutter L. Evaluati on of ISO 10272:2006 standard versus alternativ e enrichment and plating combinatio ns for enumer ation and detection of Campyl obacter in chicken meat. Food Microbiol . 2011; 28: 1117±112 3. https://doi.or g/10.1016/ j.fm.2011.03 .001 PMID: 216458 09 21. Best EL, Powell EJ, Swift C, Grant KA, Frost JA. Applicability of a rapid duplex real-time PCR assay for speciation of Campyl obacter jejuni and Campyl obacter coli directly from culture plates. FEMS Microbiol Letters. 2003; 229: 237±241 . 22. Bessede E, Solecki O, Sifre E, Labadi L, Megrau d F. Identificati on of Camp ylobacter species and related organism s by matrix assisted laser desorption ionizatio n±time of flight (MALDI-TO F) mass spectrometry. Clin Microbiol Infect. 2011; 17: 1735±9 . https://doi.or g/10.111 1/j.1469-069 1.2011.0 3468.x PMID: 213756 59 23. Dingle KE, Colles FM, Warein g DRA, Ure R, Fox AJ, Bolton FJ, et al. Multilocus sequence typing system for Campylobac ter jejuni. J Clin Microbiol . 2001; 39: 14±23. https://doi.or g/10.112 8/JCM.39 .1.1423.2001 PMID: 11136741 24. Miller WG, On SL, Wang G, Fontanoz S, Lastovica AJ, Mandre ll RE. Extended multilocus sequence typing system for Campyl obacter coli, C. lari, C. upsaliens is, and C. helveticus. J Clin Microbiol . 2005; 43: 2315±232 9. https://doi.or g/10.1128 /JCM.43.5.2 315-2329.20 05 PMID: 158722 61 25. Jolley KA, Maiden MCJ. BMC BIGSdb: Scalable analysis of bacterial genome variation at the populat ion level. Bioinfo rmatics. 2010; 11: 595. https:// doi.org/10.11 86/1471 -2105-11-595 PMID: 21143983 26. Zerbino DR, Birney E. Velvet: algorithm s for de novo short read assembly using de Bruijn graphs. Genome Res. 2008; 18: 821±829. https:// doi.org/10.11 01/gr.074 492.107 PMID: 18349386 27. Schets C, Jacobs-Reits ma WF, van der Plaats RQJ, Kerkhof-de Heer L, van Hoek AHAM, Hamidjaja RA, et al. Prevalence and types of Campylobac ter on poultry farms and in their direct environm ent. J Water Health 2017; Availab le Online 14 Septemb er 2017, wh201711 9: https:// doi.org/10.21 66/wh. 2017.119 PMID: 29215350 28. Jensen AN, Andersen MT, Dalsgaard A, Baggesen DL, Nielsen EM. Developm ent of real-time PCR and hybridiza tion methods for detection and identification of thermophilic Campylobac ter spp. in pig faecal samples . J Appl Microbiol . 2005; 99: 292±300. https://doi.or g/10.1111/j. 1365-2672.2 005.02616. x PMID: 160334 60 29. Hatta Y, Omatsu T, Tsuchiak a S, Katayama Y, Taniguch i S, Masang kay JS, et al. Detection of Campylobacter jejuni in rectal swab samples from Rousettus amplexic audatus in the Philippines. J Vet Med Sci. 2016; 78(8): 1347±1 350. https://doi.or g/10.129 2/jvms.15-06 21 PMID: 27109214 30. Adesiyun AA, Stewart-Jo hnson A, Thompson NN. Isolation of enteric pathogens from bats in Trinidad. J Wildlife Dis. 2009; 45(4): 952±96 1. Campyl obacter ssp. in bats PLOS ONE | https://doi.or g/10.137 1/journal.po ne.01906 47 January 11, 2018 9 / 10

PAGE 10

31. Veikkolai nen V, Vesterinen EJ, Lilley TM, Pulliainen AT. Bats as Reservoir Hosts of Human Bacteri al Pathogen, Bartone lla mayotim onensis. Emerg Infect Dis. 2014; 20(6): 960±7. https:// doi.org/10.32 01/ eid2006.1309 56 PMID: 24856523 32. Hazeleger WC, Jacobs-R eitsma WF, Den Besten HMW. Quantific ation of growth of Campylobac ter and extended spectrum-la ctamase produci ng bacteria sheds light on black box of enrichme nt procedures. Front Microbiol. 2016; 7: 1430. https://doi.or g/10.338 9/fmicb.2016 .01430 PMID: 27672384 33. Ivanek R, O È sterber g J, Gautam R, Sternb erg Lewerin S. Salmonella Fecal Shedding and Immune Respons es are Doseand SerotypeDependen t in Pigs. PLoS ONE 2012; 7(4): e34660. https://doi. org/10.1371/ journal.pon e.0034660 PMID: 225235 53 34. Mu È hldorfer K, Speck S, Kurth A, Lesnik R, Freuling C, Mu È ller T, et al. Disease s and causes of death in European bats: dynamics in disease susceptibility and infection rates. PLoS ONE. 2011; 6, e29773. https://doi.or g/10.137 1/journal.po ne.00297 73 PMID: 22216354 35. Reyes AW, Rovira HG, Masangka y JS, Ramirez TJ, Yoshikaw a Y, Baticados WN. Polymeras e chain reaction assay and convention al isolation of Salmon ella spp. from Philippine bats. Acta Sci Vet. 2011; 39: 947. 36. Klite P, Kourany M. Isolation of Salmonella from a neotro pical bat. J Bacteriol. 1965; 90: 831. PMID: 16562094 37. Arata AA, Vaughn JB, Newell KW, Barth RA, Gracian M. Salmon ella and Shigella infections in bats in selected areas of Columb ia. Am J Trop Med Hyg. 1968; 17: 92±5. PMID: 4866292 38. Dingle KE, Colles FM, Ure R, Wagena ar JA, Duim B, Bolton FJ, et al. Molecular character ization of Campylo bacter jejuni clones: a basis for epidemi ologic investigatio n. Emerg Infect Dis. 2002; 8: 949± 955. https://do i.org/10.3201 /eid0809. 02-0122 PMID: 12194772 39. Kwan PSL, Barrigas M, Bolton FJ, French NP, Gowlan d P, Kemp R, et al. Molecular Epidemiology of Campylo bacter jejuni Populations in Dairy Cattle, Wildlife, and the Environme nt in a Farmland Area. App Environ Microbiol . 2008; 74: 5130±8 . Campyl obacter ssp. in bats PLOS ONE | https://doi.or g/10.137 1/journal.po ne.01906 47 January 11, 2018 10 / 10


printinsert_linkshareget_appmore_horiz

Download Options [CUSTOM IMAGE]

close
No images are available for this item.
Cite this item close

APA

Cras ut cursus ante, a fringilla nunc. Mauris lorem nunc, cursus sit amet enim ac, vehicula vestibulum mi. Mauris viverra nisl vel enim faucibus porta. Praesent sit amet ornare diam, non finibus nulla.

MLA

Cras efficitur magna et sapien varius, luctus ullamcorper dolor convallis. Orci varius natoque penatibus et magnis dis parturient montes, nascetur ridiculus mus. Fusce sit amet justo ut erat laoreet congue sed a ante.

CHICAGO

Phasellus ornare in augue eu imperdiet. Donec malesuada sapien ante, at vehicula orci tempor molestie. Proin vitae urna elit. Pellentesque vitae nisi et diam euismod malesuada aliquet non erat.

WIKIPEDIA

Nunc fringilla dolor ut dictum placerat. Proin ac neque rutrum, consectetur ligula id, laoreet ligula. Nulla lorem massa, consectetur vitae consequat in, lobortis at dolor. Nunc sed leo odio.