Skip to main content
SpringerLink
Log in

Clinical infection in house rats (Rattus rattus) caused by Streptobacillus notomytis

  • Original Paper
  • Published:
Antonie van Leeuwenhoek Aims and scope Submit manuscript

Abstract

Rat bite fever is an under-reported, under-diagnosed emerging zoonosis with worldwide distribution. Besides Spirillum minus, Streptobacillus moniliformis is the major causative microorganism although it usually colonises rats without any clinical signs. A group of house rats (Rattus rattus) kept in a zoo exhibition for educational purposes suffered from neurological signs including disorientation, torticollis, stall walking, ataxia and death. Gross pathological and histo-pathological examinations of the investigated rats revealed high-grade otitis interna et media, from which Streptobacillus notomytis was isolated in pure culture or as the predominant microorganism. This case series underlines a previously expressed hypothesis that R. rattus might be naturally colonised with S. notomytis, whereas the traditional rat bite fever organism, S. moniliformis, might be restricted to the Norway rat (Rattus norvegicus). However, the general paucity of Streptobacillus isolates, especially from their respective animal hosts, precludes definitive proof of these host tropisms. This is the first report of S. notomytis detection outside Asia and Australia and the first evidence for its role as a facultative pathogen in house rats.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

Abbreviations

S. :

Streptobacillus

R. :

Rattus

RBF:

Rat bite fever

T :

Type strain

no/s.:

Number/s

m2 :

Square meter

m3 :

Cubic meter

ELISA:

Enzyme linked immunosorbent assay

Ig:

Immune globulin

µm:

Micrometer

SBA:

Columbia agar with 5% sheep blood

MALDI-TOF MS:

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

MSP:

Main spectra peak lists

MLVA:

Multi locus variable number tandem repeat analysis

groEL :

Chaperonine gene

gyrB :

Gyrase subunit B gene

recA :

Recombinase subunit A gene

mg/kg:

Milligram per kilogram

bp:

Base pair/s

SNP:

Single nucleotide polymorphism

T:

Thymine

A:

Adenine

CNS:

Central nervous system

1.0:

Male

0.1:

Female

0.0.1:

Undetermined sex

LUA:

Landesuntersuchungsanstalt für das Gesundheits- und Veterinärwesen Sachsen

LHL:

Landesbetrieb Hessisches Landeslabor

IBML:

Institut für Bakteriologie und Mykologie Leipzig

N/A:

Not applicable

EFRE:

European Funds of Regional Development

References

  • Atala A, Correa CN, Correa WM, Carrijo LN, Perfeito JB (1973) Meningitis caused by Streptobacillus moniliformis. Rev Paul Med 82:175–178

    CAS  PubMed  Google Scholar 

  • Beeuwkes H, De Jong JG, Der Van, Zalm HO (1954) Cranial base fracture with purulent meningitis due to Streptobacillus moniliformis. Ned Tijdschr Geneeskd 98:906–912

    CAS  PubMed  Google Scholar 

  • Blom J, Kreis J, Spanig S, Juhre T, Bertelli C, Ernst C, Goesmann A (2016) EDGAR 2.0: an enhanced software platform for comparative gene content analyses. Nucleic Acids Res 44:W22–W28. https://doi.org/10.1093/nar/gkw255

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Boot R, Bakker RH, Thuis H, Veenema JL, De Hoog H (1993) An enzyme-linked immunosorbent assay (ELISA) for monitoring rodent colonies for Streptobacillus moniliformis antibodies. Lab Anim 27:350–357

    Article  CAS  Google Scholar 

  • Chun J, Lee JH, Jung Y, Kim M, Kim S, Kim BK, Lim YW (2007) EzTaxon: a web-based tool for the identification of prokaryotes based on 16S ribosomal RNA gene sequences. Int J Syst Evol Microbiol 57:2259–2261. https://doi.org/10.1099/ijs.0.64915-0

    Article  CAS  Google Scholar 

  • Dijkmans BA, Thomeer RT, Vielvoye GJ, Lampe AS, Mattie H (1984) Brain abscess due to Streptobacillus moniliformis and Actinobacterium meyerii. Infection 12:262–264

    Article  CAS  Google Scholar 

  • Eisenberg T (2017) Phylogenetic investigations and comparative genome analyses within the family Leptotrichiaceae with special consideration of Streptobacillus moniliformis, the causative organism of rat bite fever. Habilitation Thesis, Justus-Liebig-University, Giessen

  • Eisenberg T, Glaeser S, Nicklas W, Mauder N, Contzen M, Aledelbi K, Kämpfer P (2015a) Streptobacillus felis sp. nov. isolated from a cat with pneumonia. Int J Syst Evol Microbiol 65:2172–2178. https://doi.org/10.1099/ijs.0.000238

    Article  CAS  PubMed  Google Scholar 

  • Eisenberg T et al (2015b) Streptobacillus notomytis sp. nov. isolated from a spinifex hopping mouse (Notomys alexis THOMAS, 1922), and emended description of Streptobacillus Levaditi et al. 1925, Eisenberg et al. 2015 emend. Int J Syst Evol Microbiol 65:4823–4829. https://doi.org/10.1099/ijsem.0.000654

    Article  CAS  PubMed  Google Scholar 

  • Eisenberg T et al (2015c) Phenotypic and genotypic characteristics of members of the genus Streptobacillus. PLoS ONE 10:e0134312. https://doi.org/10.1371/journal.pone.0134312

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Eisenberg T, Ewers C, Rau J, Akimkin V, Nicklas W (2016a) Approved and novel strategies in diagnostics of rat bite fever and other Streptobacillus infections in humans and animals Virulence 7:630–648. https://doi.org/10.1080/21505594.2016.1177694

    Article  CAS  PubMed  Google Scholar 

  • Eisenberg T, Fawzy A, Nicklas W, Semmler T, Ewers C (2016b) Phylogenetic and comparative genomics of the family Leptotrichiaceae and introduction of a novel fingerprinting MLVA for Streptobacillus moniliformis. BMC Genomics 17:864

    Article  Google Scholar 

  • Eisenberg T, Glaeser SP, Ewers C, Semmler T, Drescher B, Kämpfer P (2016c) Caviibacter abscessus gen. nov., sp. nov., a member from the family Leptotrichiaceae isolated from guinea pigs (Cavia porcellus). Int J Syst Evol Microbiol 66:1652–1659. https://doi.org/10.1099/ijsem.0.000922

    Article  CAS  PubMed  Google Scholar 

  • Eisenberg T et al (2016d) Streptobacillus ratti sp. nov., isolated from a black rat (Rattus rattus). Int J Syst Evol Microbiol 66:1620–1626. https://doi.org/10.1099/ijsem.0.000869

    Article  CAS  PubMed  Google Scholar 

  • Eisenberg T et al (2017) Acute tetraplegia caused by rat bite fever in snake keeper and transmission of Streptobacillus moniliformis. Emerg Infect Dis 23:719–721. https://doi.org/10.3201/eid2304.161987

    Article  PubMed  PubMed Central  Google Scholar 

  • Eisenberg T, Glaeser SP, Blom J, Kämpfer P (2018a) Family Leptotrichiaceae. In: Whitman WB (ed) Bergeys Manual of Systematics of Archaea and Bacteria. Wiley, New Jersey

    Google Scholar 

  • Eisenberg T, Glaeser SP, Blom J, Rau J, Kämpfer P (2018b) Genus Streptobacillus. In: Whitman WB (ed) Bergey’s Manual of Systematics of Archaea and Bacteria. Wiley, New Jersey

    Google Scholar 

  • Elliott SP (2007) Rat bite fever and Streptobacillus moniliformis. Clin Microbiol Rev 20:13–22. https://doi.org/10.1128/cmr.00016-06

    Article  PubMed  PubMed Central  Google Scholar 

  • Fornefett J et al (2017) Comparative analysis of clinics, pathologies and immune responses in BALB/c and C57BL/6J mice infected with Streptobacillus moniliformis. Microbes Infect. https://doi.org/10.1016/j.micinf.2017.10.001

    Article  PubMed  Google Scholar 

  • Fukushima K, Yanagisawa N, Imaoka K, Kimura M, Imamura A (2017) Rat-bite fever due to Streptobacillus notomytis isolated from a human specimen. J Infect Chemother. https://doi.org/10.1016/j.jiac.2017.10.018

    Article  PubMed  Google Scholar 

  • Gaastra W, Boot R, Ho HT, Lipman LJ (2009) Rat bite fever. Vet Microbiol 133:211–228. https://doi.org/10.1016/j.vetmic.2008.09.079

    Article  PubMed  Google Scholar 

  • Graves MH, Janda JM (2001) Rat-bite fever (Streptobacillus moniliformis): a potential emerging disease. Int J Infect Dis 5:151–155

    Article  CAS  Google Scholar 

  • Hill A (1974) Experimental and natural infection of the conjunctiva of rats. Lab Anim 8:305–310

    Article  CAS  Google Scholar 

  • Hopkinson WI, Lloyd JM (1981) Streptobacillus moniliformis septicaemia in spinifex hopping mice (Notomys alexis). Aust Vet J 57:533–534

    Article  CAS  Google Scholar 

  • Kearse M et al (2012) Geneious basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28:1647–1649. https://doi.org/10.1093/bioinformatics/bts199

    Article  PubMed  PubMed Central  Google Scholar 

  • Kimura M, Tanikawa T, Suzuki M, Koizumi N, Kamiyama T, Imaoka K, Yamada A (2008) Detection of Streptobacillus spp. in feral rats by specific polymerase chain reaction. Microbiol Immunol 52:9–15. https://doi.org/10.1111/j.1348-0421.2008.00005.x

    Article  CAS  PubMed  Google Scholar 

  • Koopman JP, Van den Brink ME, Vennix PP, Kuypers W, Boot R, Bakker RH (1991) Isolation of Streptobacillus moniliformis from the middle ear of rats. Lab Anim 25:35–39

    Article  CAS  Google Scholar 

  • Lane DJ (1991) 16S/23S rRNA sequencing. In: Stackebrandt E, Goodfellow M (eds) Nucleic acid techniques in bacterial systematics. Wiley, Chichester

    Google Scholar 

  • Leng-Levy J, Aubertin J, Leng B, Lacut JY, LeGall F, Emeriau J (1971) Neurologic complications of septicemias caused by Haverhillia multiformis. Lyon Med 225(Suppl):131–135

    Google Scholar 

  • Levaditi C, Nicolau S, Poincloux P (1925) Über die ätiologische Rolle von Streptobacillus moniliformis (nov. spec) bei der akuten multifokalen erythematösen Septikämie. C R Acad Sci 180:1188–1190 in Französisch

    Google Scholar 

  • Nakagomi D et al (2008) Rat-bite fever identified by polymerase chain reaction detection of Streptobacillus moniliformis DNA. J Dermatol 35:667–670. https://doi.org/10.1111/j.1346-8138.2008.00541.x

    Article  PubMed  Google Scholar 

  • Oeding P, Pedersen H (1950) Streptothrix muris ratti (Streptobacillus moniliformis) isolated from a brain abscess. Acta Pathol Microbiol Scand 27:436–442

    Article  Google Scholar 

  • Olson LD, McCune EL (1968) Histopathology of chronic otitis media in the rat. Lab Anim Care 18:478–485

    CAS  PubMed  Google Scholar 

  • Papanicolas LE, Holds JM, Bak N (2012) Meningitis and pneumonitis caused by pet rodents. Med J Aust 196:202–203

    Article  Google Scholar 

  • Pirodda E (1965) Atypical otomastoiditis due to Haverhillia multiformis (Streptobacillus moniliformis). Otorinolaringol Ital 34:23–32

    CAS  PubMed  Google Scholar 

  • Rau J, Eisenberg T, Männig A, Wind C, Lasch P, Sting R (2016) MALDI-UP—An internet platform for the exchange of MALDI-TOF mass spectra. User guide for http://maldi-up.ua-bw.de/. Aspects of food control and animal health (eJournal) 2016:1–17

  • Schuurman T, de Boer RF, Kooistra-Smid AM, van Zwet AA (2004) Prospective study of use of PCR amplification and sequencing of 16S ribosomal DNA from cerebrospinal fluid for diagnosis of bacterial meningitis in a clinical setting. J Clin Microbiol 42:734–740

    Article  CAS  Google Scholar 

  • Sens MA, Brown EW, Wilson LR, Crocker TP (1989) Fatal Streptobacillus moniliformis infection in a two-month-old infant. Am J Clin Pathol 91:612–616

    Article  CAS  Google Scholar 

  • Weisbroth SH (1979) Bacterial and mycotic diseases. In: Baker HJ, Lindsey JR, Weisbroth SH (eds) The laboratory rat—biology and diseases, vol 1. Academic Press, New York, pp 193–241

    Google Scholar 

  • Woo PC et al (2014) Streptobacillus hongkongensis sp. nov., isolated from patients with quinsy and septic arthritis, and emended descriptions of the genus Streptobacillus and the species Streptobacillus moniliformis. Int J Syst Evol Microbiol 64:3034–3039. https://doi.org/10.1099/ijs.0.061242-0

    Article  CAS  PubMed  Google Scholar 

  • Wullenweber M (1995) Streptobacillus moniliformis—a zoonotic pathogen. Taxonomic considerations, host species, diagnosis, therapy, geographical distribution. Lab Anim 29:1–15

    Article  CAS  Google Scholar 

  • Wullenweber M, Kaspareit-Rittinghausen J, Farouq M (1990) Streptobacillus moniliformis epizootic in barrier-maintained C57BL/6J mice and susceptibility to infection of different strains of mice. Lab Anim Sci 40:608–612

    CAS  PubMed  Google Scholar 

  • Wullenweber M, Jonas C, Kunstyr I (1992) Streptobacillus moniliformis isolated from otitis media of conventionally kept laboratory rats. J Exp Anim Sci 35:49–57

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The authors like to thank Anna Mohr, Marie-Luise Sonneborn, Walter Lang and Sassan Schwarz for excellent technical assistance and Ekkehard Hiller, Peter Lasch and Marcel Erhard for a helpful discussion on MALDI spectra harmonisation from different platforms. The LHL is supported by the Hessian Ministry for the Environment, Climate Change, Agriculture and Consumer Protection. The work of Juliane Fornefett, Sophie Funk and Christoph Georg Baums was financially supported by the European Funds of Regional Development (EFRE) and is registered at the “Sächsische AufbauBank” under the Proposal Number 100211188.

Author information

Authors and Affiliations

  1. Naturschutz-Tierpark Görlitz e. V., Zittauer Str. 43, 02826, Görlitz, Germany

    Viktoria Michel

  2. Landesuntersuchungsanstalt für das Gesundheits- und Veterinärwesen Sachsen (LUA), Jägerstr. 8/10, 01099, Dresden, Germany

    Claudia Ulber, Dietrich Pöhle & Beate Köpke

  3. Landesbetrieb Hessisches Landeslabor (LHL), Schubertstr. 60, 35392, Giessen, Germany

    Katharina Engel, Ute Kaim, Ahmad Fawzy & Tobias Eisenberg

  4. Faculty of Veterinary Medicine, Department of Medicine and Infectious Diseases, Cairo University, Giza Square, 12211, Egypt

    Ahmad Fawzy

  5. Veterinärmedizinische Fakultät, Zentrum für Infektionsmedizin, Institut für Bakteriologie und Mykologie, Universität Leipzig (IBML), An den Tierkliniken 29, 04103, Leipzig, Germany

    Sophie Funk, Juliane Fornefett & Christoph Georg Baums

  6. Institut für Hygiene und Infektionskrankheiten der Tiere, Justus-Liebig-Universität, Frankfurter Str. 89, 35392, Giessen, Germany

    Ahmad Fawzy & Tobias Eisenberg

Authors
  1. Viktoria Michel
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Claudia Ulber
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Dietrich Pöhle
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Beate Köpke
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Katharina Engel
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Ute Kaim
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Ahmad Fawzy
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Sophie Funk
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Juliane Fornefett
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Christoph Georg Baums
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Tobias Eisenberg
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

VM, CU, DP, BK, JF, CGB and TE made substantial contributions to conception and design or acquisition of data or analysis and interpretation of data. CU, DP, BK, KE, UK, AF, SF, JF, CGB and TE carried out diagnostics and experiments. VM was in charge of animal care, sample acquisition and therapy. TE drafted the manuscript and all the authors were involved in revising it critically for important intellectual content and approved the final version.

Corresponding author

Correspondence to Tobias Eisenberg.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed as described in Materials and Methods.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 84 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Michel, V., Ulber, C., Pöhle, D. et al. Clinical infection in house rats (Rattus rattus) caused by Streptobacillus notomytis. Antonie van Leeuwenhoek 111, 1955–1966 (2018). https://doi.org/10.1007/s10482-018-1085-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10482-018-1085-x

Keywords

Search

Navigation