An adult, male red fox (Vulpes vulpes) was found dead in a wood mid August 2010 near Nijmegen.
Photo 1 Vulpes vulpes (Photo, J. Nijendijk, Saxifraga)
Macroscopic examination The examination was hampered by the extensive autolytic changes. The fox had minor damage to its skin. It was in poor nutritional condition: it had no fat and its muscles were atrophic and pale. The external auditory canal contained a large amount of black granular material. In the middle ear and the bulla tympanica there was a small amount of clear liquid (0.5 ml). All the incisors of the upper jaw and two incisors of the lower jaw were missing. The spleen and the liver were slightly increased in size. The heart and the kidneys were pale. Multifocal red spots were observed in the cortex (outer layer) of the kidneys. There was mucopurulent material around the meninges (the membranes that cover the brain and the spinal cord) and in the cerebrospinal fluid (Photo 2). Photo 2 Inner ventral part of the skull. On the right side, the blood vessels are clear and well defined, while on the left side they are less sharp, because the mucopurulent material present. (Photo: L. Begeman, DWHC)
The meninges were thickened by deposits of fibrin (a protein originating from blood) mixed with blood and inflammatory cells. The inflammatory cells included granulocytes, lymphocytes, plasma cells, and activated histiocytes. A few calcification deposits were detected in the lung. Laboratory tests Bacteriology: The bacteria cultured from a dry swab of the brain (i.e., of the cerebrospinal fluid and meninges) included Staphylococcus pseudintermedius and Proteus sp. An antibiogram of the S.
Dutch Wildlife Health Centre (DWHC) Bacterial meningitis in a red fox 1
pseudintermedius cultured showed it was susceptible to amoxyxillin + clavulanic acid, ampicillin, cephalexin, enrofloxacin, lincomycin, tretracyclin and trimethroprim-sulfamethoxazole. Virology: The PCR for rabies on brain material, done by the CVI in Lelystad, tested negative. Cytology: Examination of the intestinal contents revealed nematode worms (Capillaria sp. and Uncinaria sp.). Conclusion
The animal had severe, subacute, extensive, mucopurulent meningitis, associated with the bacteria Staphylococcus pseudintermedius and Proteus sp. This was likely to be the primary cause of death. The origin of infection was unclear; however, the ear may be the portal of entry given the findings in the external auditory canal and in the middle ear. The malnutrition could be due to a number of reasons. Possible contributing factors are:
abnormal feeding behaviour due to the meningitis,
the gastrointestinal nematodes infestation.
Detailed examination of the gastro-intestinal tract was hampered by autolysis. There was no evidence for multi-drug resistance in the S. pseudintermedius strain isolated.
Bacterial meningitis Etiology
The causes of infection of the meninges (meningitis) include bacteria, viruses, fungi, protozoa, and parasites. In this case, the bacteria found included Staphylococcus pseudintermedius and Proteus sp. Epidemiology S. pseudintermedius en Proteus spp occur worldwide. Both are opportunistic pathogens, i.e., do not usually cause disease in healthy individuals. Staphylococcus spp. are common opportunistic pathogens that can cause serious infections in most animal species. Staphylococcus pseudintermedius has only recently been differentiated from S. aureus and other staphylococci. S. pseudintermedius is part of the normal microflora of the skin and mucosa of dogs and cats. It can cause infections of the skin and other body tissues and cavities . The genus Proteus is widespread in the environment (soil, water and manure) and is part of the normal flora of gastrointestinal tract [1, 7]. They are less frequently described as pathogens than staphylococci. As pathogens, they are mostly associated with complicated urinary tract infections, and occasionally with bacteraemia, [1, 7], wound infection, or meningitis [3, 6]. Pathogenesis and clinical findings
Bacterial meningitis often results from a direct injury, or from sinusitis or otitis. The usual signs of meningitis are:
hyperesthesia (abnormally increased sensitivity to stimuli),
paraspinal muscle (muscles next to the spine) spasms, and
photophobia (inability to tolerate light).
Dutch Wildlife Health Centre (DWHC) Bacterial meningitis in a red fox 2
Depending on the speed of onset and the site of the lesions, signs that may also be observed in diffuse meningitis are:
In dead wild animals, the diagnosis is made based on the nature of lesions observed in the meninges and the culture of bacteria from the cerebrospinal fluid. Biochemically S. pseudintermedius can be easily misidentified as S. aureus; therefore, the final microbiological identification requires genotyping [9, 10]. Management and Control
Meningitis cases caused by infection with opportunistic bacteria usually (that is, for most opportunistic bacteria species) occur as incidental cases. Therefore, though serious at the level of an individual (often fatal), they are unlikely to have an impact on the wildlife species at population level. Also humans and domestic animals can be infected by these opportunistic bacteria. Therapy may be challenging in Proteus spp. and Staphylococcus spp. infection cases, because both bacteria include strains with multidrug-resistance [5, 8, 10]. Particularly the ability of staphylococci to become resistant to antibiotics raises public health concern . Regarding Proteus sp., the level of resistance to multiple antibiotics was low in the Netherlands compared to other parts of the world . References
1. 2004. Infections of the central nervous system. 3rd ed. Scheld W.M. Whitley RJ. and Marra C.M. eds.
Lippincott Williams and Wilkins. 939 pp.
2. 2005. The Merck Veterinary Manual. 9th ed. Kahn CM. & Line S. eds. Merck & Co., Inc. 2712 pp. 3. Chuang Y. Chang W. Lu C. and Huang C. 2000. Mixed Infection in Adult Bacterial Meningitis. Infection,
4. Haesebrouck F. Devriese L.A. Vancanneyt M. Baele M. Vaneechoutte M. De Graef E. Snauwaert C.
Cleenwerck I. Dawyndt P. Swings J. and Decostere A. 2005. Staphylococcus pseudintermedius sp. nov., a coagulase-positive species from animals. Int. J. Syst. Evol. Microbiol. 55, 1569–1573.
5. Hoogkamp-Korstanje J.A.A. Roelofs-Willemse J. and The Susceptibility Surveillance Study Group. 2003.
Antimicrobial resistance in Gram-negative bacteria from Intensive Care Units and Urology Services. A nationwide study in The Netherlands 1995-2000. International journal of antimicrobial agents, 21, 6: 547-556.
6. Kassim Z. Aziz A.A. and Haque Q.M. 2003. Isolation of Proteus mirabilis from severe neonatal sepsis and
central nervous system infection with extensive pneumocephalus. European journal of pediatrics, 162, 9: 644-645.
7. Kim B.N. Kim, N.J. Kim, M.N. Kim Y.S. Woo J.H. and Ryu J. 2003. Bacteraemia due to tribe Proteeae: a
review of 132 cases during a decade (1991-2000). Scandinavian Journal of Infectious Diseases, 35, 2: 98-103. Available on:
8. Steen S. 2011. Meticillin-resistant strains of Staphylococcus pseudintermedius in companion animals.
9. Van Hoovels L. Vankeerberghen A. Boel A. Van Vaerenbergh K. and De Beenhouwer H. 2006. First
Case of Staphylococcus pseudintermedius Infection in a Human. Journal of clinical microbiology, 44, 12: 4609–4612.
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pseudintermedius in veterinary medicine. Veterinary microbiology, 140, 3-4: 418-429.
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