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Dorottya Földi Institute for Veterinary Medical Research, Centre for Agricultural Research, Hungária krt. 21, H-1143, Budapest, Hungary

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Zsuzsa Kreizinger Institute for Veterinary Medical Research, Centre for Agricultural Research, Hungária krt. 21, H-1143, Budapest, Hungary

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Katinka Bekő Institute for Veterinary Medical Research, Centre for Agricultural Research, Hungária krt. 21, H-1143, Budapest, Hungary

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Nikolett Belecz Institute for Veterinary Medical Research, Centre for Agricultural Research, Hungária krt. 21, H-1143, Budapest, Hungary

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Krisztián Bányai Institute for Veterinary Medical Research, Centre for Agricultural Research, Hungária krt. 21, H-1143, Budapest, Hungary

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Krisztián Kiss SCG Diagnostics Ltd., Délegyháza, Hungary

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Imre Biksi Department of Pathology, University of Veterinary Medicine, Budapest, Hungary

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Miklós Gyuranecz Institute for Veterinary Medical Research, Centre for Agricultural Research, Hungária krt. 21, H-1143, Budapest, Hungary

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https://orcid.org/0000-0002-5698-5713
Open access

Abstract

The control of Mycoplasma hyorhinis infection relies mainly on antimicrobial therapy. However, the antibiotic susceptibility testing of the bacteria is usually not performed before applying the treatment, and thus therapeutic failures are not uncommon. In the case of M. hyorhinis, several antibiotic-resistance-related single nucleotide polymorphisms (SNPs) are known but assays for their detection have not been described yet. The aims of the present study were to investigate macrolide- and lincomycin-resistance-related SNPs in Hungarian M. hyorhinis isolates and to develop mismatch amplification mutation assays (MAMA) to detect the identified resistance markers. Minimal inhibitory concentrations (MIC) of different drugs and whole genome sequences of 37 M. hyorhinis isolates were used to find the resistance-related mutations. One MAMA assay was designed to detect the mutation of the 23S rRNA gene at nucleotide position 2058 (Escherichia coli numbering). For further evaluation, the assay was challenged with 17 additional isolates with available MIC data and 15 DNA samples from clinical specimens. The genotypes of the samples were in line with the MIC test results. The developed assay supports the practice of targeted antibiotic usage; hence it may indirectly reduce some bacterial resistance-related public health concerns.

Abstract

The control of Mycoplasma hyorhinis infection relies mainly on antimicrobial therapy. However, the antibiotic susceptibility testing of the bacteria is usually not performed before applying the treatment, and thus therapeutic failures are not uncommon. In the case of M. hyorhinis, several antibiotic-resistance-related single nucleotide polymorphisms (SNPs) are known but assays for their detection have not been described yet. The aims of the present study were to investigate macrolide- and lincomycin-resistance-related SNPs in Hungarian M. hyorhinis isolates and to develop mismatch amplification mutation assays (MAMA) to detect the identified resistance markers. Minimal inhibitory concentrations (MIC) of different drugs and whole genome sequences of 37 M. hyorhinis isolates were used to find the resistance-related mutations. One MAMA assay was designed to detect the mutation of the 23S rRNA gene at nucleotide position 2058 (Escherichia coli numbering). For further evaluation, the assay was challenged with 17 additional isolates with available MIC data and 15 DNA samples from clinical specimens. The genotypes of the samples were in line with the MIC test results. The developed assay supports the practice of targeted antibiotic usage; hence it may indirectly reduce some bacterial resistance-related public health concerns.

Introduction

Mycoplasma hyorhinis is a facultative pathogenic Mycoplasma species causing polyserositis and arthritis in weaners and finishers from 3 to 10 weeks of age (Rovira et al., 2010). It can also induce more severe lung lesions in animals infected with Mycoplasma hyopneumoniae or porcine reproductive and respiratory syndrome virus (Lee et al., 2016; Luehrs et al., 2017). The infection results in significant economic losses worldwide (Hansen et al., 2010). A vaccine is available against M. hyorhinis infection (Ingelvac MycoMAXTM, Boehringer Ingelheim Animal Health USA Inc., Duluth, USA) in the United States, but the reduction of incidence still relies mainly on prevention by providing optimal housing conditions and the protection against other, viral pathogens (Palzer et al., 2015). A proper antibiotic treatment can decrease the severity of clinical signs of the infection and, thus, reduce the economic losses. The in vitro antibiotic susceptibility of Mycoplasma species is tested by the broth or agar microdilution method. Both methods are labour-intensive and time-consuming techniques which require the prior isolation of the pathogen. Therefore, antibiotic susceptibility testing prior to treatment is often not possible and antimicrobials are chosen empirically, which can lead to the development of antimicrobial resistance (Kobayashi et al., 2005). Further difficulties are the lack of standard breakpoints and international standards which complicate the interpretation and comparison of the results (Hannan, 2000; Kreizinger et al., 2017; Bekő et al., 2019).

Macrolide and lincosamide antimicrobials inhibit the bacterial protein synthesis by binding to the 50S subunit of the ribosome. Resistances to both of these groups are often linked because of the overlap of the binding sites at the 23S rRNA of the 50S subunit (Pyörälä et al., 2014). Mycoplasma hyorhinis is intrinsically resistant to 14-membered macrolides (Ter Laak et al., 1991; Wu et al., 2000) and a decreased susceptibility to 15- and 16-membered macrolides has also been reported (Kobayashi et al., 1996, 2005; Jang et al., 2016; Bekő et al., 2019; Rosales et al., 2020). In vitro selected resistant mutants and Japanese field isolates have been investigated for resistance-related point mutations (SNPs) in the 23S rRNA gene and the L4, L22 protein genes of the 50S ribosome by Kobayashi et al. (2005). A point mutation A2059G (according to Escherichia coli numbering) at the V domain of the 23S rRNA was found in in vitro mutants and field isolates as well. In addition, point mutations between nucleotide positions 2058 and 2062 (E. coli numbering) were connected to macrolide and lincosamide resistance in several Mycoplasma species (Sulyok et al., 2017; Chernov et al., 2018; Gautier-Bouchardon, 2018; Bekő et al., 2020a; Felde et al., 2020).

The aim of the present study was to investigate Hungarian M. hyorhinis isolates for macrolide and lincomycin resistance-related SNPs and to develop rapid and cost-effective molecular biological assays for their detection.

Materials and methods

Mycoplasma hyorhinis strains, clinical samples and susceptibility testing

In this study, 55 M. hyorhinis isolates from previous studies (Bekő et al., 2019; Földi et al., 2020) or collected in 2019–2020 and the type strain NCTC 10130 (GenBank Accession number: LS991950.1) were used. DNA extracted from the original clinical specimens of 15 clinical isolates was also examined (Supplementary Table 1). All samples originated from Hungary except for two isolates, MycSu60 and MycSu213 which originated from Slovakia. Ethical approval was not required for the study as the samples were taken either during routine diagnostic examinations with the consent of the owners or in slaughterhouses. The isolates collected in 2019–2020 were cultured as described before (Bekő et al., 2019). DNA extraction from the clinical specimens and the field isolates was performed using the QIAamp DNA Mini Kit (Qiagen Inc., Valencia, CA, USA) according to the manufacturer’s instructions for Gram-negative bacteria. All isolates were identified by polymerase chain reaction (PCR) targeting the p37 gene of M. hyorhinis (Assunção et al., 2005). The presence of other Mycoplasma species was excluded by a universal Mycoplasma PCR system targeting the 16S/23S rRNA intergenic spacer region in Mollicutes (Lauerman et al., 1995) followed by sequencing on an ABI Prism 3100 automated DNA sequencer (Applied Biosystems, Foster City, USA), then sequence analysis and BLASTN search (https://blast.ncbi.nlm.nih.gov/Blast.cgi). The DNA samples were tested for the presence of M. hyopneumoniae, Mycoplasma hyosynoviae and Mycoplasma flocculare as well by a species-specific PCR according to Assunção et al. (2005). Detailed information about the M. hyorhinis isolates used in the study can be found in Supplementary Table 1.

The antibiotic susceptibility of 38 isolates to macrolides (tylosin, tilmicosin, tylvalosin, tulathromycin, gamithromycin) and lincomycin has been previously determined by the broth microdilution method (Bekő et al., 2019) according to Hannan (2000). The susceptibility of further 17 isolates to at least one macrolide and in some cases to lincomycin was determined in this study as described before (Bekő et al., 2019). Briefly, 104 colour changing units/mL (CCU/mL) of the isolates were tested in duplicates. The antibiotics originated from VETRANAL (Sigma-Aldrich Chemie GmbH, Taufkirchen, Germany) except for tylvalosin (Aivlosin), which was purchased from ECO Animal Health Ltd. (London, UK). Stock solutions of 1 mg/mL were prepared in sterile distilled water, and stored at –70 °C, according to the recommendations of Hannan (2000). For each test, freshly prepared twofold dilutions of the antibiotics were made in the concentration range of 0.25–64 μg/mL. The M. hyorhinis type strain (NCTC 10130) was included in each plate to confirm the validity of the results. The initial minimal inhibitory concentration (MIC) of each strain was defined as the lowest concentration of the antibiotic that completely inhibited the growth at the time of colour change in the growth control. Since there are no official breakpoints available for the antibiotic susceptibility testing of M. hyorhinis, previously published breakpoints for M. hyopneumoniae or other porcine respiratory pathogens were used (Hannan et al., 1997; Felde et al., 2020; Vilaró et al., 2020). MIC values ≥4 μg/mL of tylosin, tylvalosin, gamithromycin and lincomycin were considered high (Hannan et al., 1997; Felde et al., 2020), while for tilmicosin and tulathromycin higher breakpoints were suggested, thus MIC values ≥16 μg/mL were considered high (Vilaró et al., 2020).

Development of the assay

Single nucleotide polymorphisms associated with high (genotype H) or low (genotype L) MIC values were identified by analysing the whole genome sequences of 37 M. hyorhinis field isolates and the type strain (NCTC 10130). The sequencing was performed as described before (Földi et al., 2020).

The 23S rRNA and 50S ribosomal protein L4 and L22 coding genes were previously connected to macrolide and lincomycin resistance in Mycoplasma species (Kobayashi et al., 2005; Sulyok et al., 2017; Bekő et al., 2020a; Felde et al., 2020). These genes were aligned and analysed in Geneious Prime software version 2019.2.1 (Kearse et al., 2012) to detect SNPs. In the protein-coding genes only SNPs resulting in amino acid change were analysed, but in the 23S rRNA gene all SNPs were investigated. The numbering of nucleotide position according to E. coli strain K-12 substrain MG1655 (GenBank accession number: NC_000913) is indicated in parentheses throughout the text to enable the comparison of our results with data of the literature. Nevertheless, nucleotide positions are discussed in the text based on the numbering of individual genes of the M. hyorhinis type strain (NCTC 10130) in order to avoid misunderstandings due to gaps in the alignment. To identify potentially resistance-related SNPs, the correlation between the MIC values and the occurrence of mutations were analysed. Mutations were considered resistance-related when they occurred more frequently with increasing MIC values or exclusively in isolates with high MIC values.

To detect the resistance-related SNPs, mismatch amplification mutation assays (MAMA) were designed. In brief, MAMA is a molecular biological tool to discriminate SNP in bacteria. The assay is based on competing allele-specific primers, which are SNP specific at the 3′ end and contain a single destabilising mismatch at the antepenultimate position of the 3′ end to enhance the discriminatory power. One of the allele-specific primers is marked with an additional 15- to 20-bp-long GC clamp that increases the melting temperature and the size of the amplicon as well. The temperature shift is detected on a real-time PCR platform in the presence of an intercalating fluorescent DNA dye (melt-MAMA) and the size difference is revealed in agarose gel electrophoresis (agarose-MAMA) (Birdsell et al., 2012; Sulyok et al., 2018; Bekő et al., 2020b; Felde et al., 2020). Primers were designed based on the whole genome sequences of M. hyorhinis field isolates and the type strain (NCTC 10130) in the Geneious Prime software version 2019.2.1 (Kearse et al., 2012). Melting temperatures and suitability were calculated using the NetPrimer software (Premier Biosoft International, Palo Alto, CA, USA) and the specificity of the primers was checked with BLASTN (https://blast.ncbi.nlm.nih.gov/Blast.cgi).

The agarose-MAMA PCR mixture consisted of 5 µL 5× Green GoTaq Flexi buffer (Promega Inc., Madison, WI, USA), 2.5 µL MgCl2 (25 mM; Promega), 0.5 µL dNTP (10 mM; Qiagen), 0.2 µL GoTaq Polymerase (5 U/µL, Promega), 1 µL DNA template and primers according to Table 1 with a total volume of 25 µL. The PCR was performed on a Bio-Rad C1000 TouchTM Thermal Cycler (Bio-Rad Laboratories Inc., Hercules, CA, USA). The thermocycling parameters were 95 °C for 5 min followed by 35 cycles of 95 °C for 30 s, 60 °C for 30 s and 72 °C for 30 s. The final elongation step was performed at 72 °C for 5 min. After amplification, 5 µL of each reaction mixture were submitted to electrophoresis in 3% agarose gel (MetaPhor Agarose, Lonza Inc., Rockland, ME, USA) using a 20-bp DNA ladder (O’RangeRuler 20 bp, Thermo Fisher Scientific, Waltham, USA) as a molecular weight marker. The amplified PCR products were visualised with ECO Safe Nucleic Acid Staining Solution (Pacific Image Electronics Inc., Torrance, CA, USA), under UV light. The melt-MAMA PCR mixture contained 4.5 µL 2x HSTaq Mix (PCR Biosystems Ltd., London, UK), 0.5 µL EvaGreen (20X, Biotium Inc., Hayward, USA), 1 µL target DNA and primers according to Table 1 in a final volume of 10 µL. The thermocycling parameters were 95 °C for 1 min, followed by 35 cycles of 95 °C for 15 s, 55 °C for 15 s and 72 °C for 5 s. The PCR products were subjected to melt analysis using a dissociation protocol comprising 95 °C for 15 s, followed by 0.3 °C incremental temperature ramping from 55 °C to 95 °C. The real-time PCRs were performed using Bio-Rad C1000 TouchTM Thermal Cycler, CFX96TM Real-Time System (Bio-Rad Laboratories Inc.). The EvaGreen fluorescence intensity was measured at 525 nm at each ramp interval and plotted against temperature.

Table 1.

Primer sequences, volumes per reaction and results of the designed mismatch amplification mutation assay

Primer namePrimer sequence (5′-3′)aPrimer volume (µL)bGenotypeAmplicon size (bp)Melting temperature range of amplicons (°C)
melt-MAMAagarose-MAMA
23S-LTTACCCGCATCAAGACtAA1.64L11978.3–78.9
23S-HgggcgggcgggcgggcgggcTTACCCGCATCAAGACaAg0.41H13981.3–82.2
23S-CTCCACTAGAACTAGCGTCCC0.41

a The GC-clamp, the targeted point mutation and the destabilising point mutation are in lower case; b Primer concentration: 10 pmol/μL.

Validation of the assay

In order to validate the developed assays, PCRs on 37 field isolates with already established MIC values (Bekő et al., 2019; Földi et al., 2020) were performed. The resulting genotypes (genotypes H and L) were compared with the examined gene sequence.

In order to test the sensitivity of the developed assays, tenfold dilutions of each genotype (M. hyorhinis type strain (NCTC 10130) for genotype L and MycSu24 for genotype H) were used in the range of 108–100 copy number/µL. The template copy number was calculated with the help of an online tool (Staroscik, 2004) by measuring the concentration of the DNA of pure M. hyorhinis culture by Nanodrop (2000) Spectrophotometer (Thermo Fisher Scientific). The lowest DNA concentrations detectable with agarose gel electrophoresis or yielding melting temperature specific for the genotype were considered the detection limit of the assays. The specificity was tested by including M. hyopneumoniae, M. hyosynoviae and M. flocculare in the analyses.

For further evaluation, an additional set of 17 strains was tested and the assay was also challenged with 15 DNA samples from clinical specimens. The genotypes resulting from the DNAs of the clinical specimens were compared to the genotypes of the isolates derived from these samples. The tests were considered to give false results in those cases, when the resulting genotype was not in line with the tested MIC data. For the clinical specimens the tests were considered to give false results when the resulting genotype was not in line with the genotype of the isolate derived from the sample.

Results

After aligning the corresponding genes (23S rRNA and L4, L22 50S ribosomal protein genes) of the M. hyorhinis type strain (NCTC 10130) and the 37 Hungarian field isolates, only one SNP, at nucleotide position A2066G (A2058G according to E. coli numbering), in the 23S rRNA gene (GenBank accession number: MW498281–MW498317), was found to be related to macrolide and lincomycin resistance. The primer sequences, fragment lengths and melting temperatures of the developed MAMA, specific for the SNP, are listed in Table 1. The developed assay successfully distinguished genotypes H and L (Fig. 1) in the 55 clinical isolates, the type strain (NCTC 10130) and the 15 DNA samples from the clinical materials. The sensitivity of the assay was 103 copy numbers/reaction for both genotypes in the melt and the agarose assay as well. No cross reactions were detected in the agarose-MAMA; however, M. flocculare showed a genotype L specific melting temperature profile in the melt-MAMA.

Fig. 1.
Fig. 1.

Determination of macrolide and lincomycin susceptibility by the developed MAMA assay. Melting temperatures of the amplicons for genotype L (Mycoplasma hyorhinis type strain NCTC 10130, blue line, Tm 78.6 °C) and genotype H (MycSu24, green line, Tm 81.6 °C) were unique. The negative control (black line) was not amplified. X axis: melting temperature (°C), Y axis: negative value of the change in relative fluorescence units (RFU) over the change in temperature

Citation: Acta Veterinaria Hungarica 69, 2; 10.1556/004.2021.00026

In the case of the clinical isolates, both the agarose- and the melt-MAMA gave the same results. No false reactions were detected for tylosin, tulathromycin and lincomycin. False results were detected in one case for gamithromycin (MycSu128) and tilmicosin (MycSu94) and in two cases for tylvalosin (MycSu141, MycSu161). In MycSu128, MycSu141 and MycSu161, genotype H was detected; the isolates showed elevated MIC values against five of the examined antimicrobials, but were susceptible to the remaining one. While MycSu94 was inhibited at an elevated MIC value of tilmicosin, the isolate was susceptible to all the other examined antimicrobials and presented genotype L in the assays (Supplementary Table 1).

For the clinical specimens, the test of one DNA sample (Su21) showed a mixed genotype by the agarose-MAMA, while genotype H was determined in the corresponding clinical isolate (MycSu101). The microdilution test showed elevated MIC values of the tested antibiotics against of MycSu101. At position 2066 in the whole genome sequence of this isolate, a guanine nucleotide was found, and in line with that, the assays of the pure culture resulted in genotype H. The test of the clinical specimen Su21, however, resulted in genotype L in the case of the melt-MAMA and double amplicons in the size of both genotypes appeared by the agarose-MAMA.

Discussion

The control of M. hyorhinis infections depends mainly on the use of antimicrobial agents. However, a targeted antibiotic treatment is usually inaccessible. Elevated MICs of macrolides or lincomycin to M. hyorhinis isolates have been reported from Japan, Korea, Hungary, Spain, Italy and Portugal since 1996 (Kobayashi et al., 1996, 2005; Jang et al., 2016; Bekő et al., 2019; Rosales et al., 2020), and point mutations associated with elevated MIC values were described by Kobayashi et al. (2005). In the present study, among Hungarian M. hyorhinis field isolates a transversion substitution in the previously examined region, at position 2066 (2058 E. coli numbering) of the 23S rRNA was found, an adenine was replaced by a guanine in the isolates with elevated MIC values. A mismatch amplification mutation assay was designed to detect this SNP in M. hyorhinis. The developed MAMA is suitable to detect the SNP in agarose gel based on template size differences, and in real-time PCR based on template melting temperature differences. All isolates showed uniformly high or low MIC results for all examined macrolides and lincomycin in the broth microdilution tests except for four (MycSu94, MycSu128, MycSu141, MycSu161) where the MIC of one antibiotic differed (Supplementary Table 1, highlighted with orange). Consequently, the results of the developed MAMA corresponded to the MIC values of the majority of the antibiotics in these samples. In the case of MycSu94 we assume that an evolving resistance is indicated by the elevated MIC value of tilmicosin, which did not show up in a nucleotide change at the examined position. Other SNPs or resistance mechanisms can induce the elevated MIC value, but neither can be determined based on one isolate. Against MycSu128, MycSu141 and MycSu161, we would not advise the use of macrolides, because besides the susceptibility to one of the examined macrolides, highly elevated MIC values (≥64 μg/mL) were observed for the majority of the antimicrobials. Therefore, we believe that the result of the assay (genotype H) supports the proper antibiotic treatment.

The assay is suitable for the examination of field isolates and DNA extracted directly from clinical specimens. In one case the detected genotype of the clinical specimen (in Su21 both genotypes were observed with the agarose-MAMA) differed from the genotype of the isolate that derived from it (in MycSu101 only genotype H was present). This can be explained by the filter cloning step of the isolation: in vitro testing and sequencing were made from the same one-colony broth, but based on our observation, in the clinical specimen probably more populations with different antibiotic susceptibility profiles were present.

In order to avoid the misinterpretation of the results due to the presence of M. flocculare in the melt-MAMA, we advise to submit the samples to a species-specific PCR first, and in the presence of M. flocculare only the agarose-MAMA is recommended. Clinical specimens with low specific DNA concentration (below 103 copy numbers/reaction) may show false negative results, therefore in these cases isolation prior to the test is suggested.

The developed assay is convenient, cost-effective and provides data on the susceptibility of M. hyorhinis to critically important antimicrobials in a significantly shorter time than the conventional MIC tests. The presented MAMA can be performed directly on the clinical specimens using standard laboratory equipment and methods, therefore it is suitable for routine diagnostic purposes.

Acknowledgements

This work was supported by the Lendület program (LP2012-22) of the Hungarian Academy of Sciences, the K16 (119594), FK17 (124019) and KKP19 (129751) grants of the National Research, Development and Innovation Office, Hungary. ZK and MG were supported by the Bolyai János Research Fellowship of the Hungarian Academy of Sciences. MG was supported by the Bolyai+ Fellowship (ÚNKP-19-4-ÁTE-1) of the New National Excellence Program of the Ministry of Innovation and Technology. DF was supported by the New National Excellence Program of the Ministry of Innovation and Technology (ÚNKP-20-3-I-ÁTE-4). Prepared with the professional support of the Doctoral Student Scholarship Program of the Co-operative Doctoral Program of the Ministry of Innovation and Technology, financed from the National Research, Development and Innovation Fund. The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Supplementary data to this article can be found online at https://doi.org/10.1556/004.2021.00026.

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  • Lee, J. A., Oh, Y. R., Hwang, M. A., Lee, J. B., Park, S. Y., Song, C. S., Choi, I. S. and Lee, S. W. (2016): Mycoplasma hyorhinis is a potential pathogen of porcine respiratory disease complex that aggravates pneumonia caused by porcine reproductive and respiratory syndrome virus. Vet. Immunol. Immunopathol. 177 ,4851.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Luehrs, A., Siegenthaler, S., Grützner, N., Grosse Beilage, E., Kuhnert, P. and Nathues, H. (2017): Occurrence of Mycoplasma hyorhinis infections in fattening pigs and association with clinical signs and pathological lesions of Enzootic Pneumonia. Vet. Microbiol. 203 ,15.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Palzer, A., Haedke, K., Heinritzi, K., Zoels, S., Ladinig, A. and Ritzmann, M. (2015): Associations among Haemophilus parasuis, Mycoplasma hyorhinis and porcine reproductive and respiratory syndrome virus infections in pigs with polyserositis. Can. Vet. J. 56 ,285287.

    • Search Google Scholar
    • Export Citation
  • Pyörälä, S., Baptiste, K. E., Catry, B., van Duijkeren, E., Greko, C., Moreno, M. A., Pomba, M. C. M. F., Rantala, M., Ružauskas, M., Sanders, P., Threlfall, E. J., Torren-Edo, J. and Törneke, K. (2014): Macrolides and lincosamides in cattle and pigs: Use and development of antimicrobial resistance. Vet. J. 200 ,230239.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Rosales, R. S., Ramírez, A. S., Tavío, M. M., Poveda, C. and Poveda, J. B. (2020): Antimicrobial susceptibility profiles of porcine mycoplasmas isolated from samples collected in southern Europe. BMC Vet. Res. 16 ,17.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Rovira, A., Clavijo, M. J. and Oliveira, S. (2010): Mycoplasma hyorhinis infection of pigs. Acta Sci. Vet. 38 ,Suppl. 1 ,s9s15.

  • Sulyok, K. M., Bekő, K., Kreizinger, Z., Wehmann, E., Jerzsele, Á., Rónai, Z., Turcsányi, I., Makrai, L., Szeredi, L., Jánosi, S., Nagy, S. Á. and Gyuranecz, M. (2018): Development of molecular methods for the rapid detection of antibiotic susceptibility of Mycoplasma bovis. Vet. Microbiol. 213 ,4757.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Sulyok, K. M., Kreizinger, Z., Wehmann, E., Lysnyansky, I., Bányai, K., Marton, S., Jerzsele, Á., Rónai, Z., Turcsányi, I., Makrai, L., Jánosi, S., Nagy, S. Á. and Gyuranecz, M. (2017): Mutations associated with decreased susceptibility to seven antimicrobial families in field and laboratory-derived Mycoplasma bovis strains. Antimicrob. Agents Chemother. 61 ,114.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Staroscik, A. (2004): Calculator for determining the number of copies of a template URI. Genomics Seq. Cent. http://cels.uri.edu/gsc/cndna.html.

    • Search Google Scholar
    • Export Citation
  • Ter Laak, E. A., Pijpers, A., Noordergraaf, J. H., Schoevers, E. C. and Verheijden, J. H. M. (1991): Comparison of methods for in vitro testing of susceptibility of porcine Mycoplasma species to antimicrobial agents. Antimicrob. Agents Chemother. 35 ,228233.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Vilaró, A., Novell, E., Enrique-Tarancón, V., Balielles, J., Vilalta, C., Martinez, S. and Sauce, L. J. F. (2020): Antimicrobial susceptibility pattern of porcine respiratory bacteria in Spain. Antibiotics 9 ,113.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Wu, C. C., Shryock, T. R., Lin, T. L., Faderan, M. and Veenhuizen, M. F. (2000): Antimicrobial susceptibility of Mycoplasma hyorhinis. Vet. Microbiol. 76 ,2530.

    • Crossref
    • Search Google Scholar
    • Export Citation

Supplementary Materials

  • Assunção, P., De la Fe, C., Kokotovic, B., González, O. and Poveda, J. B. (2005): The occurrence of mycoplasmas in the lungs of swine in Gran Canaria (Spain). Vet. Res. Commun. 29 ,453462.

    • Crossref
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  • Bekő, K., Felde, O., Sulyok, K. M., Kreizinger, Z., Hrivnák, V., Kiss, K., Biksi, I., Jerzsele, Á. and Gyuranecz, M. (2019): Antibiotic susceptibility profiles of Mycoplasma hyorhinis strains isolated from swine in Hungary. Vet. Microbiol. 228 ,196201.

    • Crossref
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  • Bekő, K., Kreizinger, Z., Kovács, Á. B., Sulyok, K. M., Marton, S., Bányai, K., Catania, S., Feberwee, A., Wiegel, J., Dijkman, R., ter Veen, C., Lysnyansky, I. and Gyuranecz, M. (2020a): Mutations potentially associated with decreased susceptibility to fluoroquinolones, macrolides and lincomycin in Mycoplasma synoviae. Vet. Microbiol. 248 ,https://doi.org/10.1016/j.vetmic.2020.108818.

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  • Bekő, K., Kreizinger, Z., Yvon, C., Saller, O., Catania, S., Feberwee, A. and Gyuranecz, M. (2020b): Development of molecular assays for the rapid and cost-effective determination of fluoroquinolone, macrolide and lincosamide susceptibility of Mycoplasma synoviae isolates. PLoS One 15 ,113.

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  • Birdsell, D. N., Pearson, T., Price, E. P., Hornstra, H. M., Nera, R. D., Stone, N., Gruendike, J., Kaufman, E. L., Pettus, A. H., Hurbon, A. N., Buchhagen, J. L., Harms, N. J., Chanturia, G., Gyuranecz, M., Wagner, D. M. and Keim, P. S. (2012): Melt analysis of mismatch amplification mutation assays (melt-MAMA): A functional study of a cost-effective SNP genotyping assay in bacterial models. PLoS One 7 ,https://doi.org/10.1371/journal.pone.0032866.

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  • Chernov, V. M., Chernova, O. A., Mouzykantov, A. A., Medvedeva, E. S., Baranova, N. B., Malygina, T. Y., Aminov, R. I. and Trushin, M. V. (2018): Antimicrobial resistance in mollicutes: Known and newly emerging mechanisms. FEMS Microbiol. Lett. 365 ,110.

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  • Felde, O., Kreizinger, Z., Sulyok, K. M., Wehmann, E. and Gyuranecz, M. (2020): Development of molecular biological tools for the rapid determination of antibiotic susceptibility of Mycoplasma hyopneumoniae isolates. Vet. Microbiol. 245 ,108697.

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  • Földi, D., Bekő, K., Felde, O., Kreizinger, Z., Kovács, Á. B., Tóth, F., Bányai, K., Kiss, K., Biksi, I. and Gyuranecz, M. (2020): Genotyping Mycoplasma hyorhinis by multi-locus sequence typing and multiple-locus variable-number tandem-repeat analysis. Vet. Microbiol. 249 ,https://doi.org/10.1016/j.vetmic.2020.108836.

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  • Gautier-Bouchardon, A. V. (2018): Antimicrobial resistance in Mycoplasma spp. In: Schwarz, S., Cavaco, L. M. and Shen, J. (eds) Antimicrobial Resistance in Bacteria from Livestock and Companion Animals. Wiley. pp. 425446.

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  • Hannan, P. C. T. (2000): Guidelines and recommendations for antimicrobial minimum inhibitory concentration (MIC) testing against veterinary Mycoplasma species. Vet. Res. 31 ,373395.

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  • Hannan, P. C. T., Windsor, G. D., De Jong, A., Schmeer, N. and Stegemann, M. (1997): Comparative susceptibilities of various animal-pathogenic mycoplasmas to fluoroquinolones. Antimicrob. Agents Chemother. 41 ,20372040.

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  • Hansen, M. S., Pors, S. E., Jensen, H. E., Bille-Hansen, V., Bisgaard, M., Flachs, E. M. and Nielsen, O. L. (2010): An investigation of the pathology and pathogens associated with porcine respiratory disease complex in Denmark. J. Comp. Pathol. 143 ,120131.

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  • Jang, J., Kim, K., Park, S., Park, B., Um, H., Coulier, M. and Hahn, T. W. (2016): In vitro antibiotic susceptibility of field isolates of Mycoplasma hyopneumoniae and Mycoplasma hyorhinis from Korea. Korean J. Vet. Res. 56 ,109111.

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  • Kearse, M., Moir, R., Wilson, A., Stones-Havas, S., Cheung, M., Sturrock, S., Buxton, S., Cooper, A., Markowitz, S., Duran, C., Thierer, T., Ashton, B., Meintjes, P. and Drummond, A. (2012): Geneious Basic: An integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28 ,16471649.

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  • Kobayashi, H., Morozumi, T., Miyamoto, C., Shimizu, M., Yamada, S., Ohasi, S., Kubo, M., Kimura, K., Mitani, K., Ito, N. and Yamamoto, K. (1996): Mycoplasma hyorhinis infection levels in lungs of piglets with porcine reproductive and respiratory syndrome (PRRS). J. Vet. Med. Sci. 58 ,109113.

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  • Kobayashi, H., Nakajima, H., Shimizu, Y., Eguchi, M., Hata, E. and Yamamoto, K. (2005): Macrolides and lincomycin susceptibility of Mycoplasma hyorhinis and variable mutation of domain II and V in 23S ribosomal RNA. J. Vet. Med. Sci. 67 ,795800.

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  • Kreizinger, Z., Grózner, D., Sulyok, K. M., Nilsson, K., Hrivnák, V., Benčina, D. and Gyuranecz, M. (2017): Antibiotic susceptibility profiles of Mycoplasma synoviae strains originating from Central and Eastern Europe. BMC Vet. Res. 13 ,110.

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  • Lauerman, A. L. H., Chilina, A. R., Closser, J. A. and Johansen, D. (1995): Avian Mycoplasma Identification Using Polymerase Chain Reaction Amplicon and Restriction Fragment Length Polymorphism Analysis. Published by the American Association of Avian Pathologists. Stable URL : http://www.jstor.org/stable/1592417 Linked references are: Avian Dis. 39, 804811.

    • Search Google Scholar
    • Export Citation
  • Lee, J. A., Oh, Y. R., Hwang, M. A., Lee, J. B., Park, S. Y., Song, C. S., Choi, I. S. and Lee, S. W. (2016): Mycoplasma hyorhinis is a potential pathogen of porcine respiratory disease complex that aggravates pneumonia caused by porcine reproductive and respiratory syndrome virus. Vet. Immunol. Immunopathol. 177 ,4851.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Luehrs, A., Siegenthaler, S., Grützner, N., Grosse Beilage, E., Kuhnert, P. and Nathues, H. (2017): Occurrence of Mycoplasma hyorhinis infections in fattening pigs and association with clinical signs and pathological lesions of Enzootic Pneumonia. Vet. Microbiol. 203 ,15.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Palzer, A., Haedke, K., Heinritzi, K., Zoels, S., Ladinig, A. and Ritzmann, M. (2015): Associations among Haemophilus parasuis, Mycoplasma hyorhinis and porcine reproductive and respiratory syndrome virus infections in pigs with polyserositis. Can. Vet. J. 56 ,285287.

    • Search Google Scholar
    • Export Citation
  • Pyörälä, S., Baptiste, K. E., Catry, B., van Duijkeren, E., Greko, C., Moreno, M. A., Pomba, M. C. M. F., Rantala, M., Ružauskas, M., Sanders, P., Threlfall, E. J., Torren-Edo, J. and Törneke, K. (2014): Macrolides and lincosamides in cattle and pigs: Use and development of antimicrobial resistance. Vet. J. 200 ,230239.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Rosales, R. S., Ramírez, A. S., Tavío, M. M., Poveda, C. and Poveda, J. B. (2020): Antimicrobial susceptibility profiles of porcine mycoplasmas isolated from samples collected in southern Europe. BMC Vet. Res. 16 ,17.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Rovira, A., Clavijo, M. J. and Oliveira, S. (2010): Mycoplasma hyorhinis infection of pigs. Acta Sci. Vet. 38 ,Suppl. 1 ,s9s15.

  • Sulyok, K. M., Bekő, K., Kreizinger, Z., Wehmann, E., Jerzsele, Á., Rónai, Z., Turcsányi, I., Makrai, L., Szeredi, L., Jánosi, S., Nagy, S. Á. and Gyuranecz, M. (2018): Development of molecular methods for the rapid detection of antibiotic susceptibility of Mycoplasma bovis. Vet. Microbiol. 213 ,4757.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Sulyok, K. M., Kreizinger, Z., Wehmann, E., Lysnyansky, I., Bányai, K., Marton, S., Jerzsele, Á., Rónai, Z., Turcsányi, I., Makrai, L., Jánosi, S., Nagy, S. Á. and Gyuranecz, M. (2017): Mutations associated with decreased susceptibility to seven antimicrobial families in field and laboratory-derived Mycoplasma bovis strains. Antimicrob. Agents Chemother. 61 ,114.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Staroscik, A. (2004): Calculator for determining the number of copies of a template URI. Genomics Seq. Cent. http://cels.uri.edu/gsc/cndna.html.

    • Search Google Scholar
    • Export Citation
  • Ter Laak, E. A., Pijpers, A., Noordergraaf, J. H., Schoevers, E. C. and Verheijden, J. H. M. (1991): Comparison of methods for in vitro testing of susceptibility of porcine Mycoplasma species to antimicrobial agents. Antimicrob. Agents Chemother. 35 ,228233.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Vilaró, A., Novell, E., Enrique-Tarancón, V., Balielles, J., Vilalta, C., Martinez, S. and Sauce, L. J. F. (2020): Antimicrobial susceptibility pattern of porcine respiratory bacteria in Spain. Antibiotics 9 ,113.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Wu, C. C., Shryock, T. R., Lin, T. L., Faderan, M. and Veenhuizen, M. F. (2000): Antimicrobial susceptibility of Mycoplasma hyorhinis. Vet. Microbiol. 76 ,2530.

    • Crossref
    • Search Google Scholar
    • Export Citation
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Author information is available in PDF.
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Senior editors

Editor-in-Chief: Ferenc BASKA

Editorial assistant: Szilvia PÁLINKÁS

 

Editorial Board

  • Mária BENKŐ (Acta Veterinaria Hungarica, Budapest, Hungary)
  • Gábor BODÓ (University of Veterinary Medicine, Budapest, Hungary)
  • Béla DÉNES (University of Veterinary Medicine, Budapest Hungary)
  • Edit ESZTERBAUER (Veterinary Medical Research Institute, Budapest, Hungary)
  • Hedvig FÉBEL (National Agricultural Innovation Centre, Herceghalom, Hungary)
  • László FODOR (University of Veterinary Medicine, Budapest, Hungary)
  • János GÁL (University of Veterinary Medicine, Budapest, Hungary)
  • Balázs HARRACH (Veterinary Medical Research Institute, Budapest, Hungary)
  • Peter MASSÁNYI (Slovak University of Agriculture in Nitra, Nitra, Slovak Republic)
  • Béla NAGY (Veterinary Medical Research Institute, Budapest, Hungary)
  • Tibor NÉMETH (University of Veterinary Medicine, Budapest, Hungary)
  • Zsuzsanna NEOGRÁDY (University of Veterinary Medicine, Budapest, Hungary)
  • Dušan PALIĆ (Ludwig Maximilian University, Munich, Germany)
  • Alessandra PELAGALLI (University of Naples Federico II, Naples, Italy)
  • Kurt PFISTER (Ludwig-Maximilians-University of Munich, Munich, Germany)
  • László SOLTI (University of Veterinary Medicine, Budapest, Hungary)
  • József SZABÓ (University of Veterinary Medicine, Budapest, Hungary)
  • Péter VAJDOVICH (University of Veterinary Medicine, Budapest, Hungary)
  • János VARGA (University of Veterinary Medicine, Budapest, Hungary)
  • Štefan VILČEK (University of Veterinary Medicine in Kosice, Kosice, Slovak Republic)
  • Károly VÖRÖS (University of Veterinary Medicine, Budapest, Hungary)
  • Herbert WEISSENBÖCK (University of Veterinary Medicine, Vienna, Austria)
  • Attila ZSARNOVSZKY (Szent István University, Gödöllő, Hungary)

ACTA VETERINARIA HUNGARICA
Institute for Veterinary Medical Research
Centre for Agricultural Research
Hungarian Academy of Sciences
P.O. Box 18, H-1581 Budapest, Hungary
Phone: (36 1) 287 7073 (ed.-in-chief) or (36 1) 467 4081 (editor)

E-mail: acta.veterinaria@univet.hu (ed.-in-chief)

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2022  
Web of Science  
Total Cites
WoS
972
Journal Impact Factor 0.900
Rank by Impact Factor

Veterinary Sciences 95/143

Impact Factor
without
Journal Self Cites
0.900
5 Year
Impact Factor
1.1
Journal Citation Indicator 0.47
Rank by Journal Citation Indicator

Veterinary Sciences 103/170

Scimago  
Scimago
H-index
38
Scimago
Journal Rank
0.277
Scimago Quartile Score

Veterinary (miscellaneous) Q2

Scopus  
Scopus
Cite Score
1.9
Scopus
CIte Score Rank
General Veterinary 76/186 (59th PCTL)
Scopus
SNIP
0.475

2021  
Web of Science  
Total Cites
WoS
1040
Journal Impact Factor 0,959
Rank by Impact Factor Veterinary Sciences 103/144
Impact Factor
without
Journal Self Cites
0,876
5 Year
Impact Factor
1,222
Journal Citation Indicator 0,48
Rank by Journal Citation Indicator Veterinary Sciences 106/168
Scimago  
Scimago
H-index
36
Scimago
Journal Rank
0,313
Scimago Quartile Score Veterinary (miscellaneous) (Q2)
Scopus  
Scopus
Cite Score
1,7
Scopus
CIte Score Rank
General Veterinary 79/183 (Q2)
Scopus
SNIP
0,610

2020  
Total Cites 987
WoS
Journal
Impact Factor
0,955
Rank by Veterinary Sciences 101/146 (Q3)
Impact Factor  
Impact Factor 0,920
without
Journal Self Cites
5 Year 1,164
Impact Factor
Journal  0,57
Citation Indicator  
Rank by Journal  Veterinary Sciences 93/166 (Q3)
Citation Indicator   
Citable 49
Items
Total 49
Articles
Total 0
Reviews
Scimago 33
H-index
Scimago 0,395
Journal Rank
Scimago Veterinary (miscellaneous) Q2
Quartile Score  
Scopus 355/217=1,6
Scite Score  
Scopus General Veterinary 73/183 (Q2)
Scite Score Rank  
Scopus 0,565
SNIP  
Days from  145
submission  
to acceptance  
Days from  150
acceptance  
to publication  
Acceptance 19%
Rate

 

2019  
Total Cites
WoS
798
Impact Factor 0,991
Impact Factor
without
Journal Self Cites
0,897
5 Year
Impact Factor
1,092
Immediacy
Index
0,119
Citable
Items
59
Total
Articles
59
Total
Reviews
0
Cited
Half-Life
9,1
Citing
Half-Life
9,2
Eigenfactor
Score
0,00080
Article Influence
Score
0,253
% Articles
in
Citable Items
100,00
Normalized
Eigenfactor
0,09791
Average
IF
Percentile
42,606
Scimago
H-index
32
Scimago
Journal Rank
0,372
Scopus
Scite Score
335/213=1,6
Scopus
Scite Score Rank
General Veterinary 62/178 (Q2)
Scopus
SNIP
0,634
Acceptance
Rate
18%

 

Acta Veterinaria Hungarica
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Acta Veterinaria Hungarica
Language English
Size A4
Year of
Foundation
1951
Volumes
per Year
1
Issues
per Year
4
Founder Magyar Tudományos Akadémia
Founder's
Address
H-1051 Budapest, Hungary, Széchenyi István tér 9.
Publisher Akadémiai Kiadó
Publisher's
Address
H-1117 Budapest, Hungary 1516 Budapest, PO Box 245.
Responsible
Publisher
Chief Executive Officer, Akadémiai Kiadó
ISSN 0236-6290 (Print)
ISSN 1588-2705 (Online)

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