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Cited by 9Veterinary medicine and infectious diseasesMicrobial infections and disease researchAntibiotic Use and Resistance

Temporal patterns of phenotypic antimicrobial resistance and coinfecting pathogens in Glaesserella parasuis strains isolated from diseased swine in Germany from 2006 to 2021

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Wiencek, Isabeau, Hartmann, Maria, Merkel, Jörg, Trittmacher, Sara, Kreienbrock, Lothar, Hennig-Pauka, Isabel·2022·Pathogens
DOI 10.3390/pathogens11070721PMC PMC9316560
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Abstract

Glaesserella parasuis (Gps) causes high economic losses in pig farms worldwide. So far no vaccine provides cross-protection for different serotypes, so antibiotic treatment is widely used to cope with this pathogen. In this study, routine diagnostic data from 2046 pigs with Gps related diseases sent for necropsy to a German laboratory in the time period 2006–2021 were analysed retrospectively. In the time period 2018–2021, the most frequent serotypes (ST) detected were ST4 (30%) and ST13 (22%). A comparison of the reference period 2006–2013 prior to obligatory routine recording of antimicrobial usage in livestock with the period 2014–2021 resulted in a statistically significant decrease of frequencies of resistant Gps isolates for ceftiofur, enrofloxacin, erythromycin, spectinomycin, tiamulin and tilmicosin. While in 2006–2013 all isolates were resistant for tetracyclin and cephalothin, frequencies of resistant isolates decreased in the second time period to 28% and 62%, respectively. Parallel to the reduction of antimicrobial usage, during recent years a reduction in resistant Gps isolates has been observed, so only a low risk of treatment failure exists. Most frequently, pigs positive for Gps were also positive for S.suis (25.4%), PRRSV-EU (25.1%) and influenza virus (23%). The viral pathogens may act as potential trigger factors.

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  1. [2]Howell K.J. Peters S.E. Wang J. Hernandez-Garcia J. Weinert L.A. Luan S.L. Chaudhuri R.R. Angen Ø. Aragon V. Williamson S.M. Development of a Multiplex PCR Assay for Rapid Molecular Serotyping of Haemophilus parasuis J. Clin. Microbiol. 2015 53 3812 3821 10.1128/JCM.01991-15 26424843 PMC4652097 · DOI
  2. [3]Kielstein P. Rapp-Gabrielson V.J. Designation of 15 serovars of Haemophilus parasuis on the basis of immunodiffusion using heat-stable antigen extracts J. Clin. Microbiol. 1992 30 862 865 10.1128/jcm.30.4.862-865.1992 1572971 PMC265175 · DOI
  3. [4]Zhang P. Zhang C. Aragon V. Zhou X. Zou M. Wu C. Shen Z. Investigation of Haemophilus parasuis from healthy pigs in China Vet. Microbiol. 2019 231 40 44 10.1016/j.vetmic.2019.02.034 30955821 · DOI
  4. [5]Pereira D. Dalla-Costa F. Ferroni L. Moraes C. Schocken-Iturrino R. Oliveira L. The challenges with Glässer’s disease in technified pig production Austral J. Vet. Sci. 2017 49 63 69 10.4067/S0719-81322017000200063 · DOI
  5. [6]Schuwerk L. Hoeltig D. Waldmann K.H. Strutzberg-Minder K. Valentin-Weigand P. Rohde J. Serotyping and pathotyping of Glaesserella parasuis isolated 2012-2019 in Germany comparing different PCR-based methods Vet. Res. 2020 51 137 10.1186/s13567-020-00862-1 33203465 PMC7673094 · DOI
  6. [7]Galofré-Milà N. Correa-Fiz F. Lacouture S. Gottschalk M. Strutzberg-Minder K. Bensaid A. Pina-Pedrero S. Aragon V. A robust PCR for the differentiation of potential virulent strains of Haemophilus parasuis BMC Vet. Res. 2017 13 124 10.1186/s12917-017-1041-4 28482900 PMC5422950 · DOI
  7. [8]Olvera A. Cerdà-Cuéllar M. Aragon V. Study of the population structure of Haemophilus parasuis by multilocus sequence typing Microbiology 2006 152 3683 3690 10.1099/mic.0.29254-0 17159221 · DOI
  8. [10]Correa-Fiz F. Fraile L. Aragon V. Piglet nasal microbiota at weaning may influence the development of Glässer’s disease during the rearing period BMC Genom. 2016 17 404 10.1186/s12864-016-2700-8 PMC4881051 27230662 · DOI
  9. [11]Samuelson D.R. Welsh D.A. Shellito J.E. Regulation of lung immunity and host defense by the intestinal microbiota Front. Microbiol. 2015 6 1085 10.3389/fmicb.2015.01085 26500629 PMC4595839 · DOI
  10. [12]Charlson E.S. Bittinger K. Haas A.R. Fitzgerald A.S. Frank I. Yadav A. Bushman F.D. Collman R.G. Topographical continuity of bacterial populations in the healthy human respiratory tract Am. J. Respir. Crit. Care Med. 2011 184 957 963 10.1164/rccm.201104-0655OC 21680950 PMC3208663 · DOI · Paper page
  11. [13]Rogers G.B. The lung microbiome Emerg. Top. Life Sci. 2017 1 313 324 10.1042/etls20170043 33525774 · DOI
  12. [14]Kernaghan S. Bujold A.R. MacInnes J.I. The microbiome of the soft palate of swine Anim. Health Res. Rev. 2012 13 110 120 10.1017/S1466252312000102 22853946 · DOI
  13. [15]Lowe B.A. Marsh T.L. Isaacs-Cosgrove N. Kirkwood R.N. Kiupel M. Mulks M.H. Defining the “core microbiome” of the microbial communities in the tonsils of healthy pigs BMC Microbiol. 2012 12 20 10.1186/1471-2180-12-20 22313693 PMC3297519 · DOI
  14. [17]Bello-Orti B. Deslandes V. Tremblay Y.D. Labrie J. Howell K.J. Tucker A.W. Maskell D.J. Aragon V. Jacques M. Biofilm formation by virulent and non-virulent strains of Haemophilus parasuis Vet. Res. 2014 45 104 10.1186/s13567-014-0104-9 25428823 PMC4245831 · DOI
  15. [18]Jiang R. Xiang M. Chen W. Zhang P. Wu X. Zhu G. Tu T. Jiang D. Yao X. Luo Y. Biofilm characteristics and transcriptomic analysis of Haemophilus parasuis Vet. Microbiol. 2021 258 109073 10.1016/j.vetmic.2021.109073 33984794 · DOI
  16. [19]Macedo N. Cheeran M.C. Rovira A. Holtcamp A. Torremorell M. Effect of enrofloxacin on Haemophilus parasuis infection, disease and immune response Vet. Microbiol. 2017 199 91 99 10.1016/j.vetmic.2016.12.032 28110792 · DOI
  17. [20]Hemme M. Ruddat I. Hartmann M. Werner N. van Rennings L. Käsbohrer A. Kreienbrock L. Antibiotic use on German pig farms—A longitudinal analysis for 2011, 2013 and 2014 PLoS ONE 2018 13 e0199592 10.1371/journal.pone.0199592 29969477 PMC6029768 · DOI
  18. [21]Schaekel F. May T. Seiler J. Hartmann M. Kreienbrock L. Antibiotic drug usage in pigs in Germany-Are the class profiles changing? PLoS ONE 2017 12 e0182661 10.1371/journal.pone.0182661 28841685 PMC5571922 · DOI
  19. [23]van Rennings L. von Münchhausen C. Ottilie H. Hartmann M. Merle R. Honscha W. Käsbohrer A. Kreienbrock L. Cross-sectional study on antibiotic usage in pigs in Germany PLoS ONE 2015 10 e0119114 10.1371/journal.pone.0119114 25785688 PMC4364977 · DOI
  20. [24]Vahle J.L. Haynes J.S. Andrews J.J. Experimental reproduction of Haemophilus parasuis infection in swine: Clinical, bacteriological, and morphologic findings J. Vet. Diagn. Investig. 1995 7 476 480 10.1177/104063879500700409 8580168 · DOI
  21. [25]Vahle J.L. Haynes J.S. Andrews J.J. Interaction of Haemophilus parasuis with nasal and tracheal mucosa following intranasal inoculation of cesarean derived colostrum deprived (CDCD) swine Can. J. Vet. Res. 1997 61 200 206 9243000 PMC1189404
  22. [26]Wang H. Wei W. Cao Q. Xu M. Chen Q. Lv Y. Tan C. Dai M. Xu X. Chen H. Sialylated Lipooligosaccharide Contributes to Glaesserella parasuis Penetration of Porcine Respiratory Epithelial Barrier ACS Infect. Dis. 2021 7 661 671 10.1021/acsinfecdis.0c00850 33645216 · DOI
  23. [27]Costa-Hurtado M. Ballester M. Galofré-Milà N. Darji A. Aragon V. VtaA8 and VtaA9 from Haemophilus parasuis delay phagocytosis by alveolar macrophages Vet. Res. 2012 43 57 10.1186/1297-9716-43-57 22839779 PMC3462726 · DOI
  24. [28]Olvera A. Ballester M. Nofrarías M. Sibila M. Aragon V. Differences in phagocytosis susceptibility in Haemophilus parasuis strains Vet. Res. 2009 40 24 10.1051/vetres/2009007 19239855 PMC2695031 · DOI
  25. [29]Olvera A. Pina S. Pérez-Simó M. Oliveira S. Bensaid A. Virulence-associated trimeric autotransporters of Haemophilus parasuis are antigenic proteins expressed in vivo Vet. Res. 2010 41 26 10.1051/vetres/2009074 19995512 PMC2820231 · DOI
  26. [30]Pina S. Olvera A. Barceló A. Bensaid A. Trimeric autotransporters of Haemophilus parasuis: Generation of an extensive passenger domain repertoire specific for pathogenic strains J. Bacteriol. 2009 191 576 587 10.1128/JB.00703-08 19011035 PMC2620822 · DOI
  27. [31]Wan X. Wang G. Gao W. Li C. Yan H. Comparative genome analysis of multidrug-resistant and susceptible Glaesserella parasuis strains isolated from diseased pigs in China Vet. Microbiol. 2021 254 109002 10.1016/j.vetmic.2021.109002 33610012 · DOI
  28. [32]Zhang K. Chu P. Song S. Yang D. Bian Z. Li Y. Gou H. Jiang Z. Cai R. Li C. Proteome Analysis of Outer Membrane Vesicles From a Highly Virulent Strain of Haemophilus parasuis Front. Vet. Sci. 2021 8 756764 10.3389/fvets.2021.756764 34901247 PMC8662722 · DOI
  29. [33]Macedo N. Gottschalk M. Strutzberg-Minder K. Van C.N. Zhang L. Zou G. Zhou R. Marostica T. Clavijo M.J. Tucker A. Molecular characterization of Glaesserella parasuis strains isolated from North America, Europe and Asia by serotyping PCR and LS-PCR Vet. Res. 2021 52 68 10.1186/s13567-021-00935-9 33980312 PMC8117636 · DOI
  30. [35]Burow E. Kasbohrer A. Risk Factors for Antimicrobial Resistance in Escherichia coli in Pigs Receiving Oral Antimicrobial Treatment: A Systematic Review Microb. Drug Resist. 2017 23 194 205 10.1089/mdr.2015.0318 27249658 · DOI
  31. [36]Dorey L. Pelligand L. Cheng Z. Lees P. Pharmacokinetic/pharmacodynamic integration and modelling of florfenicol for the pig pneumonia pathogens Actinobacillus pleuropneumoniae and Pasteurella multocida PLoS ONE 2017 12 e0177568 10.1371/journal.pone.0177568 28552968 PMC5446118 · DOI
  32. [37]de la Fuente A.J. Tucker A.W. Navas J. Blanco M. Morris S.J. Gutiérrez-Martín C.B. Antimicrobial susceptibility patterns of Haemophilus parasuis from pigs in the United Kingdom and Spain Vet. Microbiol. 2007 120 184 191 10.1016/j.vetmic.2006.10.014 17110059 · DOI
  33. [38]El Garch F. de Jong A. Simjee S. Moyaert H. Klein U. Ludwig C. Marion H. Haag-Diergarten S. Richard-Mazet A. Thomas V. Monitoring of antimicrobial susceptibility of respiratory tract pathogens isolated from diseased cattle and pigs across Europe, 2009–2012: VetPath results Vet. Microbiol. 2016 194 11 22 10.1016/j.vetmic.2016.04.009 27102206 · DOI
  34. [40]Li J. Wang S. Li C. Wang C. Liu Y. Wang G. He X. Hu L. Liu Y. Cui M. Secondary Haemophilus parasuis infection enhances highly pathogenic porcine reproductive and respiratory syndrome virus (HP-PRRSV) infection-mediated inflammatory responses Vet. Microbiol. 2017 204 35 42 10.1016/j.vetmic.2017.03.035 28532803 · DOI
  35. [41]Costa-Hurtado M. Barba-Vidal E. Maldonado J. Aragon V. Update on Glässer’s disease: How to control the disease under restrictive use of antimicrobials Vet. Microbiol. 2020 242 108595 10.1016/j.vetmic.2020.108595 32122599 · DOI
  36. [42]Hau S.J. Eberle K.C. Brockmeier S.L. Importance of strain selection in the generation of heterologous immunity to Glaesserella (Haemophilus) parasuis Vet. Immunol. Immunopathol. 2021 234 110205 10.1016/j.vetimm.2021.110205 33636545 · DOI
  37. [43]Liu H. Xue Q. Zeng Q. Zhao Z. Haemophilus parasuis vaccines Vet. Immunol. Immunopathol. 2016 180 53 58 10.1016/j.vetimm.2016.09.002 27692096 · DOI
  38. [44]Blanco-Fuertes M. Correa-Fiz F. López-Serrano S. Sibila M. Aragon V. Sow vaccination against virulent Glaesserella parasuis shapes the nasal microbiota of their offspring Sci. Rep. 2022 12 3357 10.1038/s41598-022-07382-2 35233006 PMC8888576 · DOI
  39. [45]López-Serrano S. Neila-Ibáñez C. Costa-Hurtado M. Mahmmod Y. Martínez-Martínez J. Galindo-Cardiel I.J. Darji A. Rodríguez F. Sibila M. Aragon V. Sow vaccination with a protein fragment against virulent Glaesserella (Haemophilus) parasuis modulates immunity traits in their offspring Vaccines 2021 9 534 10.3390/vaccines9050534 34065547 PMC8160652 · DOI
  40. [46]Oliveira S. Pijoan C. Haemophilus parasuis: New trends on diagnosis, epidemiology and control Vet. Microbiol. 2004 99 1 12 10.1016/j.vetmic.2003.12.001 15019107 · DOI
  41. [47]Saade G. Deblanc C. Bougon J. Marois-Créhan C. Fablet C. Auray G. Belloc C. Leblanc-Maridor M. Gagnon C.A. Zhu J. Coinfections and their molecular consequences in the porcine respiratory tract Vet. Res. 2020 51 80 10.1186/s13567-020-00807-8 32546263 PMC7296899 · DOI
  42. [48]Mathieu-Denoncourt A. Letendre C. Auger J.P. Segura M. Aragon V. Lacouture S. Gottschalk M. Limited interactions between Streptococcus suis and Haemophilus parasuis in in vitro co-infection studies Pathogens 2018 7 7 10.3390/pathogens7010007 PMC5874733 29316613 · DOI
  43. [49]Yu J. Wu J. Zhang Y. Guo L. Cong X. Du Y. Li J. Sun W. Shi J. Peng J. Concurrent highly pathogenic porcine reproductive and respiratory syndrome virus infection accelerates Haemophilus parasuis infection in conventional pigs Vet. Microbiol. 2012 158 316 321 10.1016/j.vetmic.2012.03.001 22460022 · DOI
  44. [50]Liu S. Li W. Wang Y. Gu C. Liu X. Charreyre C. Fan S. He Q. Coinfection with Haemophilus parasuis serovar 4 increases the virulence of porcine circovirus type 2 in piglets Virol. J. 2017 14 227 10.1186/s12985-017-0890-6 29157279 PMC5696968 · DOI
  45. [51]Dubosson C.R. Conzelmann C. Miserez R. Boerlin P. Frey J. Zimmermann W. Häni H. Kuhnert P. Development of two real-time PCR assays for the detection of Mycoplasma hyopneumoniae in clinical samples Vet. Microbiol. 2004 102 55 65 10.1016/j.vetmic.2004.05.007 15288927 · DOI
  46. [52]Luehrs A. Siegenthaler S. Grützner N. Grosse Beilage E. Kuhnert P. Nathues H. Occurrence of Mycoplasma hyorhinis infections in fattening pigs and association with clinical signs and pathological lesions of Enzootic Pneumonia Vet. Microbiol. 2017 203 1 5 10.1016/j.vetmic.2017.02.001 28619130 · DOI
  47. [53]Brunborg I.M. Moldal T. Jonassen C.M. Quantitation of porcine circovirus type 2 isolated from serum/plasma and tissue samples of healthy pigs and pigs with postweaning multisystemic wasting syndrome using a TaqMan-based real-time PCR J. Virol. Methods 2004 122 171 178 10.1016/j.jviromet.2004.08.014 15542141 · DOI
  48. [54]Tabynov K. Sansyzbay A. Tulemissova Z. Tabynov K. Dhakal S. Samoltyrova A. Renukaradhya G.J. Mambetaliyev M. Inactivated porcine reproductive and respiratory syndrome virus vaccine adjuvanted with Montanide™ Gel 01 ST elicits virus-specific cross-protective inter-genotypic response in piglets Vet. Microbiol. 2016 192 81 89 10.1016/j.vetmic.2016.06.014 27527768 PMC7111292 · DOI
  49. [55]Goodell C.K. Zhang J. Strait E. Harmon K. Patnayak D. Otterson T. Culhane M. Christopher-Hennings J. Clement T. Leslie-Steen P. Ring test evaluation of the detection of influenza A virus in swine oral fluids by real-time reverse-transcription polymerase chain reaction and virus isolation Can. J. Vet. Res. 2016 80 12 20 26733728 PMC4686030
  50. [61]Dayao D.A. Kienzle M. Gibson J.S. Blackall P.J. Turni C. Use of a proposed antimicrobial susceptibility testing method for Haemophilus parasuis Vet. Microbiol. 2014 172 586 589 10.1016/j.vetmic.2014.06.010 24984947 · DOI

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Authors
Wiencek, I., Hartmann, M., Merkel, J., Trittmacher, S., Kreienbrock, L., & Hennig-Pauka, I.
Affiliations
  • University of Veterinary Medicine Hannover, Foundation (DE)
  • Field Station for Epidemiology, University of Veterinary Medicine Hannover, 49456 Bakum, Germany
ORCID
Venue
Pathogens
Publisher
MDPI AG
Published
2022-06-24
Volume
11
Issue
7
Pages
721
ISSN
2076-0817 (ISSN-L)
DOI
10.3390/pathogens11070721
PMC
PMC9316560
OpenAlex
W4283590914
Cited by
9
References
1
Citations by year
2026: 4 · 2025: 3 · 2023: 2
FWCI
1.38
Type
journal article
Language
en
Open access
Licence
Locations
  • Pathogens (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders
Deutsche Forschungsgemeinschaft (DFG, German Research Foundation) (491094227)
Topics
  • Health Sciences › Veterinary › Small Animals › Veterinary medicine and infectious diseases
  • Life Sciences › Immunology and Microbiology › Microbiology › Microbial infections and disease research
  • Life Sciences › Immunology and Microbiology › Applied Microbiology and Biotechnology › Antibiotic Use and Resistance
Keywords
Haemophilus parasuis, antimicrobial resistance, pigs, serotypes, co-infection, porcine circovirus type 2, porcine reproductive and respiratory syndrome virus, influenza virus, ceftiofur, enrofloxacin, erythromycin, tetracycline, tiamulin, tilmicosin, antimicrobial use, temporal trends

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