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      MLST-based genetic relatedness of Campylobacter jejuni isolated from chickens and humans in Poland

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      Journal: PLoS ONE
      Publisher: Public Library of Science

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          Abstract

          Campylobacter jejuni infection is one of the most frequently reported foodborne bacterial diseases worldwide. The main transmission route of these microorganisms to humans is consumption of contaminated food, especially of chicken origin. The aim of this study was to analyze the genetic relatedness of C. jejuni from chicken sources (feces, carcasses, and meat) and from humans with diarrhea as well as to subtype the isolates to gain better insight into their population structure present in Poland. C. jejuni were genotyped using multilocus sequence typing (MLST) and sequence types (STs) were assigned in the MLST database. Among 602 isolates tested, a total of 121 different STs, including 70 (57.9%) unique to the isolates' origin, and 32 STs that were not present in the MLST database were identified. The most prevalent STs were ST464 and ST257, with 58 (9.6%) and 52 (8.6%) C. jejuni isolates, respectively. Isolates with some STs (464, 6411, 257, 50) were shown to be common in chickens, whereas others (e.g. ST21 and ST572) were more often identified among human C. jejuni. It was shown that of 47 human sequence types, 26 STs (106 isolates), 23 STs (102 isolates), and 29 STs (100 isolates) were also identified in chicken feces, meat, and carcasses, respectively. These results, together with the high and similar proportional similarity indexes (PSI) calculated for C. jejuni isolated from patients and chickens, may suggest that human campylobacteriosis was associated with contaminated chicken meat or meat products or other kinds of food cross-contaminated with campylobacters of chicken origin. The frequency of various sequence types identified in the present study generally reflects of the prevalence of STs in other countries which may suggest that C. jejuni with some STs have a global distribution, while other genotypes may be more restricted to certain countries.

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          Multilocus sequence typing system for Campylobacter jejuni.

          K Dingle, F. Colles, D Wareing … (2001)
          The gram-negative bacterium Campylobacter jejuni has extensive reservoirs in livestock and the environment and is a frequent cause of gastroenteritis in humans. To date, the lack of (i) methods suitable for population genetic analysis and (ii) a universally accepted nomenclature has hindered studies of the epidemiology and population biology of this organism. Here, a multilocus sequence typing (MLST) system for this organism is described, which exploits the genetic variation present in seven housekeeping loci to determine the genetic relationships among isolates. The MLST system was established using 194 C. jejuni isolates of diverse origins, from humans, animals, and the environment. The allelic profiles, or sequence types (STs), of these isolates were deposited on the Internet (http://mlst.zoo.ox.ac.uk), forming a virtual isolate collection which could be continually expanded. These data indicated that C. jejuni is genetically diverse, with a weakly clonal population structure, and that intra- and interspecies horizontal genetic exchange was common. Of the 155 STs observed, 51 (26% of the isolate collection) were unique, with the remainder of the collection being categorized into 11 lineages or clonal complexes of related STs with between 2 and 56 members. In some cases membership in a given lineage or ST correlated with the possession of a particular Penner HS serotype. Application of this approach to further isolate collections will enable an integrated global picture of C. jejuni epidemiology to be established and will permit more detailed studies of the population genetics of this organism.
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            Campylobacters as zoonotic pathogens: a food production perspective.

            Tom Humphrey, Sarah E O'Brien, Mogens Madsen (2007)
            Campylobacters remain highly important zoonotic pathogens worldwide which infect an estimated 1% of the population of Western Europe each year. Certain campylobacters are also important in infections of animals, particularly of the reproductive tract, and some are involved in periodontal disease. This paper focuses, however, on the two species which are most important in food-borne infections of humans, Campylobacter (C.) jejuni and C. coli. Infection with these campylobacters is serious in its own right but can also have long-term sequelae such as reactive arthritis and Guillain-Barré syndrome. The pathogens are ubiquitous in nature and in domestic animals and, as a consequence, are found frequently in the environment and on many raw foods, of both plant and animal origin and bacterial numbers can be very high on certain key foods like raw poultry meat. Although all commercial poultry species can carry campylobacters, the risk is greater from chicken because of the high levels of consumption. Campylobacters are relatively 'new' zoonotic pathogens as routine culture from clinical specimens only became possible in the late 1970s. As a consequence there is much that still needs to be understood about the behaviour and pathogenicity of these highly important bacteria. In particular, and from a food industry/food safety perspective, it is important to better understand the behaviour of C. jejuni and C. coli in the food production environment, and how this affects their ability to survive certain food production processes. There is a belief that campylobacters are much more sensitive to hostile conditions than either salmonellas or Escherichia coli. Much of data to support this view have been derived from laboratory experiments and may not fully represent the natural situation. Studies are showing that campylobacters may be more robust than previously thought and thus may represent a greater challenge to food safety. We recommend that research is undertaken to better understand how campylobacters behave in the food chain and how responses to relevant conditions affect their ability to survive processing and their virulence. There is also a need to better understand the reasons why campylobacters are capable of frequent change, particularly in the expression of surface antigens.
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              Assigning the source of human campylobacteriosis in New Zealand: a comparative genetic and epidemiological approach.

              Petra Müllner, Simon E.F. Spencer, Daniel J Wilson … (2009)
              Integrated surveillance of infectious multi-source diseases using a combination of epidemiology, ecology, genetics and evolution can provide a valuable risk-based approach for the control of important human pathogens. This includes a better understanding of transmission routes and the impact of human activities on the emergence of zoonoses. Until recently New Zealand had extraordinarily high and increasing rates of notified human campylobacteriosis, and our limited understanding of the source of these infections was hindering efforts to control this disease. Genetic and epidemiological modeling of a 3-year dataset comprising multilocus sequence typed isolates from human clinical cases, coupled with concurrent data on food and environmental sources, enabled us to estimate the relative importance of different sources of human disease. Our studies provided evidence that poultry was the leading cause of human campylobacteriosis in New Zealand, causing an estimated 58-76% of cases with widely varying contributions by individual poultry suppliers. These findings influenced national policy and, after the implementation of poultry industry-specific interventions, a dramatic decline in human notified cases was observed in 2008. The comparative-modeling and molecular sentinel surveillance approach proposed in this study provides new opportunities for the management of zoonotic diseases.
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                Author and article information

                Contributors
                Kinga Wieczorek: Role: ConceptualizationRole: Formal analysisRole: InvestigationRole: MethodologyRole: ValidationRole: Writing – original draftRole: Writing – review & editing
                Tomasz Wołkowicz: Role: InvestigationRole: Writing – review & editing
                Jacek Osek:
                ORCID: http://orcid.org/0000-0003-2295-8837
                Role: ConceptualizationRole: Formal analysisRole: Funding acquisitionRole: InvestigationRole: MethodologyRole: Project administrationRole: SupervisionRole: ValidationRole: Writing – original draftRole: Writing – review & editing
                Patrick Jon Biggs: Role: Editor
                Journal
                Journal ID (nlm-ta): PLoS One
                Journal ID (iso-abbrev): PLoS ONE
                Journal ID (publisher-id): plos
                Journal ID (pmc): plosone
                Title: PLoS ONE
                Publisher: Public Library of Science (San Francisco, CA USA )
                ISSN (Electronic): 1932-6203
                Publication date (Electronic): 24 January 2020
                Publication date Collection: 2020
                Volume: 15
                Issue: 1
                Electronic Location Identifier: e0226238
                Affiliations
                [1 ] Department of Hygiene of Food of Animal Origin, National Veterinary Research Institute, Pulawy, Poland
                [2 ] Department of Bacteriology and Biocontamination Control, National Institute of Public Health—National Institute of Hygiene, Warsaw, Poland
                Massey University, NEW ZEALAND
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Author information
                http://orcid.org/0000-0003-2295-8837
                Article
                Publisher ID: PONE-D-18-24292
                DOI: 10.1371/journal.pone.0226238
                PMC ID: 6980552
                PubMed ID: 31978059
                SO-VID: d3d53028-cfb2-4600-9695-57cdbeee8273
                Copyright © © 2020 Wieczorek et al
                License:

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                Date received : 24 August 2018
                Date accepted : 24 November 2019
                Page count
                Figures: 1, Tables: 4, Pages: 13
                Funding
                Funded by: funder-id http://dx.doi.org/10.13039/501100004281, Narodowe Centrum Nauki;
                Award ID: UMO-2014/15/B/NZ7/00874
                Award Recipient :
                ORCID: http://orcid.org/0000-0003-2295-8837
                Funded by: European Union
                Award ID: 773830
                Award Recipient :
                This study was financially supported by National Science Centre, Poland, on the basis of Decision UMO-2014/15/B/NZ7/00874 (JO). The present work was in part supported by the One Health EJP project that has received funding from the European Union’s Horizon 2020 research and innovation programme under grant agreement No 773830 (2018-2022) (KW). Both funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Subject: Research Article
                Subject: Biology and Life Sciences
                Subject: Organisms
                Subject: Eukaryota
                Subject: Animals
                Subject: Vertebrates
                Subject: Amniotes
                Subject: Birds
                Subject: Fowl
                Subject: Gamefowl
                Subject: Chickens
                Subject: Biology and Life Sciences
                Subject: Organisms
                Subject: Eukaryota
                Subject: Animals
                Subject: Vertebrates
                Subject: Amniotes
                Subject: Birds
                Subject: Poultry
                Subject: Chickens
                Subject: Biology and Life Sciences
                Subject: Agriculture
                Subject: Animal Products
                Subject: Meat
                Subject: Biology and Life Sciences
                Subject: Nutrition
                Subject: Diet
                Subject: Food
                Subject: Meat
                Subject: Medicine and Health Sciences
                Subject: Nutrition
                Subject: Diet
                Subject: Food
                Subject: Meat
                Subject: Biology and Life Sciences
                Subject: Organisms
                Subject: Bacteria
                Subject: Campylobacter
                Subject: Biology and Life Sciences
                Subject: Microbiology
                Subject: Medical Microbiology
                Subject: Microbial Pathogens
                Subject: Bacterial Pathogens
                Subject: Campylobacter
                Subject: Medicine and Health Sciences
                Subject: Pathology and Laboratory Medicine
                Subject: Pathogens
                Subject: Microbial Pathogens
                Subject: Bacterial Pathogens
                Subject: Campylobacter
                Subject: Research and Analysis Methods
                Subject: Database and Informatics Methods
                Subject: Biological Databases
                Subject: Sequence Databases
                Subject: Research and Analysis Methods
                Subject: Database and Informatics Methods
                Subject: Bioinformatics
                Subject: Sequence Analysis
                Subject: Sequence Databases
                Subject: People and places
                Subject: Geographical locations
                Subject: Europe
                Subject: European Union
                Subject: Poland
                Subject: Medicine and Health Sciences
                Subject: Infectious Diseases
                Subject: Bacterial Diseases
                Subject: Campylobacteriosis
                Subject: Biology and Life Sciences
                Subject: Organisms
                Subject: Bacteria
                Subject: Campylobacter
                Subject: Campylobacter Jejuni
                Subject: Biology and Life Sciences
                Subject: Microbiology
                Subject: Medical Microbiology
                Subject: Microbial Pathogens
                Subject: Bacterial Pathogens
                Subject: Campylobacter
                Subject: Campylobacter Jejuni
                Subject: Medicine and Health Sciences
                Subject: Pathology and Laboratory Medicine
                Subject: Pathogens
                Subject: Microbial Pathogens
                Subject: Bacterial Pathogens
                Subject: Campylobacter
                Subject: Campylobacter Jejuni
                Subject: Medicine and Health Sciences
                Subject: Gastroenterology and Hepatology
                Subject: Diarrhea
                Subject: Medicine and Health Sciences
                Subject: Diagnostic Medicine
                Subject: Signs and Symptoms
                Subject: Diarrhea
                Subject: Medicine and Health Sciences
                Subject: Pathology and Laboratory Medicine
                Subject: Signs and Symptoms
                Subject: Diarrhea
                Custom metadata
                Data Availability All relevant data are within the paper and its Supporting Information files.

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