Skip to main content
Download PDF

Studies on Trueperella pyogenes isolated from an okapi (Okapia johnstoni) and a royal python (Python regius)

BMC Veterinary Research volume 16, Article number: 292 (2020) Cite this article

Abstract

Background

The present study was designed to characterize phenotypically and genotypically two Trueperella pyogenes strains isolated from an okapi (Okapia johnstoni) and a royal python (Python regius).

Case presentation

The species identity could be confirmed by phenotypic properties, by MALDI-TOF MS analysis and by detection of T. pyogenes chaperonin-encoding gene cpn60 with a previously developed loop-mediated isothermal amplification (LAMP) assay. Furthermore, sequencing of the 16S ribosomal RNA (rRNA) gene, the 16S-23S rDNA intergenic spacer region (ISR), the target genes rpoB encoding the β-subunit of bacterial RNA polymerase, tuf encoding elongation factor tu and plo encoding the putative virulence factor pyolysin allowed the identification of both T. pyogenes isolates at species level.

Conclusions

Both strains could be clearly identified as T. pyogenes. The T. pyogenes strain isolated in high number from the vaginal discharge of an okapi seems to be of importance for the infectious process; the T. pyogenes strain from the royal python could be isolated from an apparently non-infectious process. However, both strains represent the first isolation of T. pyogenes from these animal species.

Background

Trueperella pyogenes is worldwide considered as part of the commensal biota of skin and mucous membranes of the upper respiratory and urogenital tract of animals [1]. However, T. pyogenes is also an important opportunistic pathogen that causes mastitis, abortion and a variety of diverse pyogenic infections in livestock, including cattle, sheep, goats, horses, and pigs [2,3,4]. In cattle, T. pyogenes appears to be responsible for infections of the reproductive tract [5] and the mammary gland [6], as well as cases of pneumonia and liver abscessation of large and small ruminants [7]. In swine, T. pyogenes is well known as a causative agent of different types of inflammation in various organs including the lung, heart, joints, mammary glands, and in the reproductive tract [8, 9]. Furthermore, T. pyogenes could be found in companion animals [4]. One of the first reported cases in companion animals was an otitis externa detected in a cat and cystitis in a dog [10]. More recently, Wareth et al. [11] described a co-infection case of T. pyogenes with Brucella abortus in a cat and dog. Additionally, various wildlife animals could harbour T. pyogenes [3]. In 2010, Ülbegi-Mohyla et al. [12] characterized two T. pyogenes strains isolated from a bearded dragon and a gecko. Additionally, T. pyogenes infections were reported from a bison and from camels [13, 14], from goitered gazelles [15] and from a white-tailed deer [16]. Likewise, some other sporadic cases of infectious diseases associated with T. pyogenes were described in a galago [17], in gray slender lorises [18, 19] and in a eurasian lynx [20].

Besides conventional bacteriological methods for identifying T. pyogenes isolates, other new, fast and reliable techniques were described and utilized in this study: matrix-assisted laser desorption/ionization time-of-flight mass spectrometry (MALDI-TOF MS) [20,21,22,23], a loop-mediated isothermal amplification (LAMP) assay [24] and 16S rRNA gene sequencing [25, 26].

The present study was designed to identify and further characterize T. pyogenes isolated from wildlife animals phenotypically and genotypically. To the best of our knowledge, the present study provides a first detailed description of T. pyogenes recovered from an okapi and a royal python.

Case presentation

As part of routine examination and diagnostics performed on zoo animals at Frankfurt Zoo (Frankfurt am Main, Germany) in 2019, T. pyogenes 24398 was isolated from a vaginal discharge of an okapi (Okapia johnstoni) in high numbers (+++), together with Enterobacter cloacae (+) and Pasteurella spp. (+). The initial bacteriology analysis for T. pyogenes 24398 was performed at Hessian State Laboratory (LHL) Gießen, Germany. As a result of post-mortem examination conducted in 2017, T. pyogenes 171003246 was recovered in low numbers (+) from a kidney of a seven-year-old female royal python (Python regius). The python was found dead in a bird park in Hesse (Germany) and was 107 cm in length and weighted 1.23 kg. In addition, Escherichia coli (+), α-hemolytic streptococci (+), Corynebacterium spp. (+) and Clostridium sardiniense (+) were cultured from the python specimen. The post-mortem analysis of the royal python revealed a good body condition and in the throat and head area a 15 cm lung edema and swelling, possibly caused by traumatic reasons. The post-mortem examination and the initial bacteriology analysis were also performed at Hessian State Laboratory. Both T. pyogenes strains were further investigated phenotypically and genotypically.

Phenotypic characterization

A phenotypic characterization was performed using conventional cultural and biochemical assays as previously described [12, 18, 20, 27] and the API-Coryne test System (BioMérieux, Nürtingen, Germany) in accordance with the manufacturer’s instructions. Furthermore, the bacterial isolates were identified by MALDI-TOF MS using a Microflex LT (Bruker Daltonik GmbH, Bremen, Germany) instrument and MBT Compass Explorer 4.1 software (Bruker Daltonik GmbH). Sample preparation was carried out in accordance with the manufacturer’s instructions using the direct transfer method. Briefly, one microbial colony was first smeared in duplicate onto spots of the MALDI target MSP 96 target (MicroScout Target plate; Bruker Daltonik GmbH) with sterile toothpicks. The air-dried bacteria were overlaid with 1 µl of an α-cyan 4-hydroxycinnamic acid matrix solution (HCCA, in 50% acetonitrile and 2.5% trifluoroacetic acid in pure water) followed by drying and loading into the mass spectrometer.

Genotypic properties

The genomic DNA of both isolates and the type strains T. pyogenes DSM 20630T (pig), T. abortisuis DSM 19515T (placenta of sow after abortion), T. bernardiae DSM 9152T (human blood) and T. bonasi DSM 17163T (european bison) were extracted using the DNeasy blood and tissue kit (Qiagen GmbH, Hilden, Germany), in accordance with the manufacturer’s instructions. The concentration and purity of DNA were measured by utilizing a Nano Drop spectrophotometer (ND1000; Thermo Fisher Scientific GmbH, Dreieich, Germany).

The detection of gene cpn60 of T. pyogenes was performed using a previously designed loop-mediated isothermal amplification (LAMP) assay [24] with a portable real-time fluorometer (Genie II®, OptiGene Ltd, Horsham, UK) and the reference strains T. pyogenes DSM 20630T, T. abortisuis DSM 19515T, T. bernardiae DSM 9152T and T. bonasi DSM 17163T.

Both T. pyogenes isolates were also evaluated by PCR for the presence of five genomic targets: 16S rRNA gene (16S), 16S-23S rDNA intergenic spacer region (ISR), the β-subunit of bacterial RNA polymerase encoding gene rpoB, the elongation factor tu encoding gene tuf, and pyolysin encoding gene plo. The sequence of the oligonucleotide primers and PCR conditions were previously described by Hassan et al. [25], Ülbegi-Mohyla et al. [12], Hijazin et al. [27], Eisenberg et al. [18], Wickhorst et al. [28], Wickhorst et al. [23], Alssahen et al. [20].

The PCR products were purified and sequenced by Eurofins Umwelt Nord GmbH (Göttingen, Germany). The obtained sequences were analyzed via the cluster method of the MegAlign program (DNASTAR Inc., ver. 15, Madison, WI, USA) by comparing with the nucleotide sequences of 16S rRNA, ISR, rpoB, tuf and plo from different Trueperella reference strains. Moreover, the resulting amino acid sequences of pyolysin of both T. pyogenes isolates were compared with the respective sequences of pyolysin of T. pyogenes DSM 20630T, closely related pore-forming toxins of genus Arcanobacterium and with other bacterial pore-forming toxins. All the nucleotide and amino acid sequences were obtained from the NCBI GenBank.

Discussion and Conclusion

Both T. pyogenes strains investigated in the present study showed a narrow zone of complete hemolysis on 5% sheep blood agar and CAMP-like reactions in the staphylococcal β-hemolysin zone with Rhodococcus hoagii as an indicator strain. The conventional biochemical properties and the results of the commercial identification system revealed almost identical results to previously investigated T. pyogenes of various origins and T. pyogenes DSM 20630T [12, 18, 20, 27] (Table. 1). The T. pyogenes isolates yielded positive reactions for pyrrolidonyl arylamidase, alkaline phosphatase, β-glucuronidase, β-galactosidase, α-glucosidase and N-acetyl-β-glucosaminidase and negative reactions for nitrate reduction and pyrazinamidase. Additionally, the isolates hydrolyzed gelatine, but not esculin and urea. The isolates also fermented D-glucose, D-ribose, D-xylose, D-maltose, D-lactose and glycogen, but not D-mannitol. T. pyogenes 24398 fermented D-saccharose; however, T. pyogenes 171003246 was D-saccharose negative. In addition, both isolates showed a negative catalase reaction and a positive reaction on Löffler agar (Table 1). A postitive reaction on Löffler agar is typical for T. pyogenes and widely used for phenotypic identification of this species [2, 18].

Table 1 Biochemical properties of T. pyogenes 24398 (okapi), T. pyogenes 171003246 (royal python) and type strain T. pyogenes DSM 20630T
Full size table

Moreover, MALDI-TOF MS identified T. pyogenes 24398 and T. pyogenes 171003246 with log score values of 2.35 and 2.29 for the first hit and log score values of 2.28 and 1.9 for the second hit, respectively (data not shown). These log score values confirmed, in accordance with the current decision rules of the manufacturer, the species designation. Comparable to the present results, MALDI-TOF MS had already been shown to be a rapid and reliable technique for identifying bacteria of genera Arcanobacterium and Trueperella, including T. pyogenes [20, 21].

The previously described cpn60-specific LAMP assay could successfully be used to identify the species-specific gene cpn60 of T. pyogenes 24,398 and T. pyogenes 171,003,246 in the present investigation. This was comparable to the LAMP assay for detecting gene cpn60 of the previously described T. pyogenes of various origins [24], a T. pyogenes strain isolated from an adult roebuck (Capreolus capreolus) [23], and a T. pyogenes strain isolated from a eurasian lynx (Lynx lynx) [20]. The results of the cpn60 LAMP assay are shown in Fig. 1; Table 2.

Fig. 1
figure 1

Positive LAMP assay of T. pyogenes 24398 (okapi), T. pyogenes 171003246 (royalpython), T. pyogenes DSM 20630T, the LAMP negative control strains T. abortisuis DSM 19515T, T. bernardiaeDSM 9152Tand T. bonasi DSM 17163T, and a negative control

Full size image
Table 2 Results of LAMP including detection time and annealing temperature of the tested isolate, positive and negative control
Full size table

The oligonucleotide primers, 16SUNI-L and 16SUNI-R, were used for amplifying of 16S rRNA gene of the investigated T. pyogenes isolates. The nucleotide sequence data of T. pyogenes 24398 (GenBank accession numbers: MN946520) and T. pyogenes 171003246 (MN712476) were compared with type strain T. pyogenes DSM 20630T (AAC45754) and with the previously described strain T. pyogenes S 1276/1/18 isolated from a eurasian lynx (MN135984), T. abortisuis DSM 19515T (FN667628), T. bernardiae DSM 9152T (X79224), T. bialowiezensis DSM 17162T (EU194569), and T. bonasi DSM 17163T (EU194570). The nucleotide sequence data of T. pyogenes 24398 and T. pyogenes 171003246 revealed a sequence homology of 98.9% among both strains, a sequence homology of 99.5% and 98.7% with T. pyogenes DSM 20,630T, and a sequence homology of 99.9% and 99.1% with T. pyogenes S1276/1/18, respectively. The control strains of genus Trueperella yielded a sequence homology to both T. pyogenes isolates ≤ 98.7% (Fig. 2).

Fig. 2
figure 2

Phylogenetic analysis based on nucleotide sequences of 16S rRNA gene of the investigated T. pyogenes 24398 and T. pyogenes 171003246 isolated from okapi and royal python compared with the type strain T. pyogenes DSM 20630T and T. pyogenes S 1276/1/18 isolated from a eurasian lynx, T. abortisuis DSM 19515T, T. bernardiae DSM 9152T, T. bialowiezensis DSM 17162T, and T. bonasi DSM 17163T

Full size image

Both strains T. pyogenes 24398 and T. pyogenes 171003246 were further identified by sequencing ISR, the genes tuf and rpoB and the putative virulence factor pyolysin encoding gene plo. T. pyogenes 24398 and T. pyogenes 171003246 showed sequence similarities of ISR (MN947249, MN724920) of 99.8% and 98.9% with T. pyogenes DSM 20630T (EU194563) and 100% and 99.8% with T. pyogenes S 1276/1/18 (MN164031), respectively with 98.5% identity between both strains. The additionally investigated gene tuf (MN956808, MN741111) showed a sequence similarity of 99.6% and 99.7% with T. pyogenes DSM 20630T (HG941716), and 99.6% and 99.7% with T. pyogenes S 1276/1/18 (MN163266), respectively; gene rpoB (MN956807, MN741109), a sequence similarity of 99.8% and 98.3% with T. pyogenes DSM 20630T (FN550375), and 98.8% and 98.3% with T. pyogenes S 1276/1/18 (MN163265), respectively, and gene plo (MN956806, MN741110), a sequence similarity of 99.5% with T. pyogenes DSM 20630T (U84782) for both isolates, and 99.1% with T. pyogenes S 1276/1/18 (MN163264) for both isolates.

Dendrograms of the ISR, tuf and rpoB genes are presented in Fig. 3.

Fig. 3
figure 3

Phylogenetic analyses based on ISR (a), tuf (b) and ropB (c) nucleotide sequences of the investigated T. pyogenes 24398 and T. pyogenes 171003246 and T. pyogenes S 1276/1/18 isolated from a eurasian lynx and the control strains, T. pyogenes DSM 20630T, T. abortisuis DSM 19515T, T. bernardiae DSM 9152T, T. bialowiezensis DSM 17162T, and T. bonasi DSM 17163T

Full size image

A phylogenetic analysis of the amino acid sequences of pyolysin (PLO) encoded by gene plo of T. pyogenes 24398 (MN956806), and T. pyogenes 171003246 (MN741110) PLO of type strain T. pyogenes DSM 20630T (AAC45754), PLO of T. pyogenes S 1276/1/18 (MN163264), arcanolysin (ALN) of Arcanobacterium haemolyticum (ACV96715), phocaelysin (PHL) of Arcanobacterium phocae 10002T (SMR98720), listeriolysin O (HLY) of Listeria monocytogenes (NP_463733), intermedilysin (ILY) of Streptococcus intermedius (BAA89790), pneumolysin (PLY) of Streptococcus pneumoniae (ADF28298) and streptolysin O (SLO) of Streptococcus pyogenes (BAB41212). The results showed an amino acid similarity of 99.5% for both T. pyogenes 24,398 and T. pyogenes 171003246 with PLO of T. pyogenes DSM 20630T and 99.1% with PLO of T. pyogenes S 1276/1/18 (Fig. 4).

Fig. 4
figure 4

Phylogenetic relationships among amino acid sequences of PLO of the investigated T. pyogenes 24398 and T. pyogenes 171003246, PLO of type strain T. pyogenes 20630T, T. pyogenes S 1276/1/18 isolated from a eurasian lynx, ALN of A. haemolyticum, PHL of A. phocae, HLY of L. monocytogenes, PLY of S. pneumoniae

Full size image

T. pyogenes 24398 was isolated in high numbers from vaginal discharge of an okapi and seems to be responsible for the infectious process; T. pyogenes 171003246 was isolated from a non-infectious process of a royal python suffering from a throat swelling, possibly caused by trauma. Both T. pyogenes isolates were identified by a biochemical test, LAMP and MALDI-TOF MS. The genomic targets of the two isolates, 16S rRNA gene, ISR, tuf, rpoB and plo were sequenced and compared to the respective targets of reference and other strains. Thus, the report is the first to provide a detailed characterization of T. pyogenes strains of these origin.

Availability of data and materials

The datasets generated during the current study are available in the NBCI GenBank repository, under the accession number: MN741109, MN741110, MN741111, MN956806, MN956807 and MN956808.

Abbreviations

MALDI-TOF MS:

Matrix-assisted laser desorption/ionization time-of-flight mass spectrometry

LAMP:

Loop-mediated isothermal amplification

rRNA:

Ribosomal RNA

ISR:

16S-23S rDNA intergenic spacer region

CAMP test:

Christie-Atkins-Munch-Peterson-test

DSM:

German Collection of Microorganisms

ALN:

Arcanolysin

PHL:

Phocaelysin

HLY:

Listeriolysin O

ILY:

Intermedilysin

PLY:

Pneumolysin

SLO:

Streptolysin O

References

  1. Rzewuska M, Kwiecien E, Chrobak-Chmiel D, Kizerwetter-Swida M, Stefanska I, Gierynska M. Pathogenicity and virulence of Trueperella pyogenes: a review. Int J Mol Sci. 2019;20(11):2737.

  2. Lämmler C, Hartwigk H. Actinomyces pyogenes und Arcanobacterium haemolyticum. In: Handbuch der bakteriellen Infektionen bei Tieren. 2nd edn: Gustav Fischer: Jena 1995: 196–240.

  3. Jost BH, Billington SJ. Arcanobacterium pyogenes: molecular pathogenesis of an animal opportunist. Antonie Van Leeuwenhoek. 2005;88(2):87–102.

    Article  PubMed  Google Scholar 

  4. Ribeiro MG, Risseti RM, Bolanos CAD, Caffaro KA, de Morais ACB, Lara GHB, et al. Trueperella pyogenes multispecies infections in domestic animals: a retrospective study of 144 cases (2002 to 2012). Vet Quart. 2015;35(2):82–7.

    Article  CAS  Google Scholar 

  5. Tamai IA, Mohammadzadeh A, Salehi TZ, Mahmoodi P. Genomic characterisation, detection of genes encoding virulence factors and evaluation of antibiotic resistance of Trueperella pyogenes isolated from cattle with clinical metritis. Antonie Van Leeuwenhoek. 2018;111(12):2441–53.

    Article  Google Scholar 

  6. Ishiyama D, Mizomoto T, Ueda C, Takagi N, Shimizu N, Matsuura Y, et al. Factors affecting the incidence and outcome of Trueperella pyogenes mastitis in cows. J Vet Med Sci. 2017;79(3):626–31.

    Article  PubMed  PubMed Central  Google Scholar 

  7. Rogovskyy AS, Lawhon S, Kuczmanski K, Gillis DC, Wu J, Hurley H, et al. Phenotypic and genotypic characteristics of Trueperella pyogenes isolated from ruminants. J Vet Diagn Invest. 2018;30(3):348–53.

    Article  PubMed  PubMed Central  Google Scholar 

  8. Jarosz LS, Gradzki Z, Kalinowski M. Trueperella pyogenes infections in swine: clinical course and pathology. Pol J Vet Sci. 2014;17(2):395–404.

    Article  PubMed  CAS  Google Scholar 

  9. Dong WL, Liu L, Odah KA, Atiah LA, Gao YH, Kong LC, et al. Antimicrobial resistance and presence of virulence factor genes in Trueperella pyogenes isolated from pig lungs with pneumonia. Trop Anim Health Pro. 2019;51(7):2099–103.

    Article  Google Scholar 

  10. Billington SJ, Post KW, Jost BH. Isolation of Arcanobacterium (Actinomyces) pyogenes from cases of feline otitis externa and canine cystitis. J Vet Diagn Invest. 2002;14(2):159–62.

    Article  PubMed  CAS  Google Scholar 

  11. Wareth G, El-Diasty M, Melzer F, Murugaiyan J, Abdulmawjood A, Sprague LD, et al. Trueperella pyogenes and Brucella abortus coinfection in a dog and a cat on a dairy farm in Egypt with recurrent cases of mastitis and abortion. Vet Med Int. 2018;2018:2056436.

  12. Ülbegi-Mohyla H, Hijazin M, Alber J, Lämmler C, Hassan AA, Abdulmawjood A, et al. Identification of Arcanobacterium pyogenes isolated by post mortem examinations of a bearded dragon and a gecko by phenotypic and genotypic properties. J Vet Sci. 2010;11(3):265–7.

    Article  PubMed  PubMed Central  Google Scholar 

  13. Wareth G, Murugaiyan J, Khater DF, Moustafa SA. Subclinical pulmonary pathogenic infection in camels slaughtered in Cairo, Egypt. J Infect Dev Countr. 2014;8(7):909–13.

    Article  Google Scholar 

  14. Tarazi YH, Al-Ani FK. An outbreak of dermatophilosis and caseous lymphadenitis mixed infection in camels (Camelus dromedaries) in Jordan. J Infect Dev Countr. 2016;10(5):506–11.

    Article  CAS  Google Scholar 

  15. Ҫeҫen G, Buyukcangaz EK, Caliskan UG, Cangul TI, Akdesir E. Interdigital necrobacillosis associated with Trueperella pyogenes in Goitered Gazelles (Gazella Subgutturosa). J Zoo Wildlife Med. 2018;49(2):429–34.

  16. Cohen BS, Belser EH, Keeler SP, Yabsley MJ, Miller KV. Isolation and genotypic characterization of Trueperella (Arcanobacterium) pyogenes recovered from active cranial abscess Infections of Male White-Tailed Deer (Odocoileus Virginianus). J Zoo Wildlife Med. 2015;46(1):62–7.

    Article  Google Scholar 

  17. Salleng KJ, Burton BJ, Apple TM, Sanchez S. Isolation of Trueperella pyogenes in a case of thoracic and abdominal abscess in a galago (Otolemur garnettii). J Med Primatol. 2016;45(4):198–201.

    Article  PubMed  Google Scholar 

  18. Eisenberg T, Nagib S, Hijazin M, Alber J, Lämmler C, Hassan AA, et al. Trueperella pyogenes as cause of a facial abscess in a grey slender loris (Loris lydekkerianus nordicus) - a case report. Berl Münch Tierärztl. 2012;125(9–10):407–10.

    Google Scholar 

  19. Nagib S, Glaeser SP, Eisenberg T, Sammra O, Lämmler C, Kämpfer P, et al. Fatal infection in three Grey Slender Lorises (Loris lydekkerianus nordicus) caused by clonally related Trueperella pyogenes. BMC Vet Res. 2017;13:273.

    Article  PubMed  PubMed Central  Google Scholar 

  20. Alssahen M, Peters M, Rau J, Hassan AA, Sammra O, Lämmler C, et al. Phenotypic and genotypic approach to characterize a Trueperella pyogenes strain isolated from an Eurasian Lynx (Lynx lynx). Berl Münch Tierärztl. 2020. https://doi.org/10.2376/0005-9366-19037.

    Article  Google Scholar 

  21. Hijazin M, Hassan AA, Alber J, Lämmler C, Timke M, Kostrzewa M, et al. Evaluation of matrix-assisted laser desorption ionization-time of flight mass spectrometry (MALDI-TOF MS) for species identification of bacteria of genera Arcanobacterium and Trueperella. Vet Microbiol. 2012;157(1–2):243–5.

    Article  PubMed  CAS  Google Scholar 

  22. Randall LP, Lemma F, Koylass M, Rogers J, Ayling RD, Worth D, et al. Evaluation of MALDI-TOF as a method for the identification of bacteria in the veterinary diagnostic laboratory. Res Vet Sci. 2015;101:42–9.

    Article  PubMed  CAS  Google Scholar 

  23. Wickhorst JP, Hassan AA, Sheet OH, Eisenberg T, Sammra O, Alssahen M, et al. Trueperella pyogenes isolated from a brain abscess of an adult roebuck (Capreolus capreolus). Folia Microbiol. 2018;63(1):17–22.

    Article  CAS  Google Scholar 

  24. Abdulmawjood A, Wickhorst J, Hashim O, Sammra O, Hassan AA, Alssahen M, et al. Application of a loop-mediated isothermal amplification (LAMP) assay for molecular identification of Trueperella pyogenes isolated from various origins. Mol Cell Probe. 2016;30(4):205–10.

    Article  CAS  Google Scholar 

  25. Hassan AA, Ülbegi-Mohyla H, Kanbar T, Alber J, Lämmler C, Abdulmawjood A, et al. Phenotypic and genotypic characterization of Arcanobacterium haemolyticum isolates from infections of horses. J Clin Microbiol. 2009;47(1):124–8.

    Article  PubMed  CAS  Google Scholar 

  26. Moreno LZ, Matajira CEC, da Costa BLP, Ferreira TSP, Silva GFR, Dutra MC, et al. Characterization of porcine Trueperella pyogenes by matrix-assisted laser desorption ionization-time of flight mass spectrometry (MALDI-TOF MS), molecular typing and antimicrobial susceptibility profiling in Sao Paulo State. Comp Immunol Microb. 2017;51:49–53.

    Article  Google Scholar 

  27. Hijazin M, Ülbegi-Mohyla H, Alber J, Lämmler C, Hassan AA, Abdulmawjood A, et al. Molecular identification and further characterization of Arcanobacterium pyogenes isolated from bovine mastitis and from various other origins. J Dairy Sci. 2011;94(4):1813–9.

    Article  PubMed  CAS  Google Scholar 

  28. Wickhorst JP, Sammra O, Hassan AA, Alssashen M, Lämmler C, Prenger-Berninghoff E, et al. Identification of Arcanobacterium hippocoleae by MALDI-TOF MS analysis and by various genotypical properties. Res Vet Sci. 2017;115:10–2.

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

Not applicable.

Funding

Open access funding provided by Projekt DEAL.

Author information

Authors and Affiliations

  1. Hygiene and Zoonoses Department, Faculty of Veterinary Medicine, Mansoura University, Elgomhoria Street 60, 35516, Mansoura, Egypt

    Marwa F. E. Ahmed

  2. Institut für Hygiene und Infektionskrankheiten der Tiere, Justus-Liebig-Universität Gießen, Frankfurterstraße 85-91, D-35392, Gießen, Germany

    Mazen Alssahen & Christoph Lämmler

  3. Landesbetrieb Hessisches Landeslabor (LHL), Schubertstraße 60, D-35392, Gießen, Germany

    Tobias Eisenberg

  4. Institute of Food Quality and Food Safety, Research Center for Emerging Infections and Zoonoses (RIZ), University of Veterinary Medicine Hannover, Bischofsholer Damm 15, D-30173, Hannover, Germany

    Madeleine Plötz & Amir Abdulmawjood

Authors
  1. Marwa F. E. Ahmed
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Mazen Alssahen
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Christoph Lämmler
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Tobias Eisenberg
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Madeleine Plötz
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Amir Abdulmawjood
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

MFEA, MA, CL, AA and MP contributed to the design of the study, collected and analysed the data. TE performed the initial examination of the isolates. MFEA, AA and MP drafted the manuscript. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Amir Abdulmawjood.

Ethics declarations

Ethics approval and consent to participate

This study did not require official or institutional ethical approval. The material was collected post mortem and/or during routine diagnosis. According to competent authorities, this kind of research does not require ethics approval or general approval with respect to German law.

Consent for publication

Not applicable.

Competing interests

The authors declare that they have no competing interests.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ahmed, M.F., Alssahen, M., Lämmler, C. et al. Studies on Trueperella pyogenes isolated from an okapi (Okapia johnstoni) and a royal python (Python regius). BMC Vet Res 16, 292 (2020). https://doi.org/10.1186/s12917-020-02508-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1186/s12917-020-02508-y

Keywords

BMC Veterinary Research

ISSN: 1746-6148

Contact us