Highly Pathogenic Avian Influenza Virus (H5N1) Infection in Red Foxes Fed Infected Bird Carcasses

Leslie A. Reperant; Geert van Amerongen; Marco W.G. van de Bildt; Guus F. Rimmelzwaan; Andrew P. Dobson; Albert D.M.E. Osterhaus; Thijs Kuiken


Emerging Infectious Diseases. 2008;14(12):1835-1841. 

In This Article

Abstract and Introduction


Eating infected wild birds may put wild carnivores at high risk for infection with highly pathogenic avian influenza (HPAI) virus (H5N1). To determine whether red foxes (Vulpes vulpes) are susceptible to infection with HPAI virus (H5N1), we infected 3 foxes intratracheally. They excreted virus pharyngeally for 3-7 days at peak titers of 103.5-105.2 median tissue culture infective dose (TCID50) per mL and had severe pneumonia, myocarditis, and encephalitis. To determine whether foxes can become infected by the presumed natural route, we fed infected bird carcasses to 3 other red foxes. These foxes excreted virus pharyngeally for 3-5 days at peak titers of 104.2-104.5 TCID50/mL, but only mild or no pneumonia developed. This study demonstrates that red foxes fed bird carcasses infected with HPAI virus (H5N1) can excrete virus while remaining free of severe disease, thereby potentially playing a role in virus dispersal.


Influenza A viruses rarely infect species of the order Carnivora. However, since 2003, highly pathogenic avian influenza (HPAI) viruses of subtype H5N1 have infected a wide range of carnivore species. Within the past 30 years, and before the emergence of HPAI viruses (H5N1), 5 documented outbreaks of influenza virus infections occurred in 2 carnivore species—the harbor seal (Phoca vitulina),[1,2,3,4] and the American mink (Mustela vison).[5] In both species, the infection resulted in respiratory disease. In addition, influenza virus infection has been detected by virus culture or serologic examination in other carnivores, namely, domestic dogs (Canis lupus familiaris),[6,7] domestic cats (Felis catus),[8,9] and bears kept in captivity (species not stated);[9] however, these animals did not show clinical signs of disease. Also, recently, outbreaks of equine influenza virus (H3N8) infections resulted in respiratory disease in domestic dogs.[10,11] In contrast, within the past 5 years, HPAI viruses (H5N1) have infected and killed carnivores belonging to 7 species: captive tigers (Panthera tigris) and leopards (P. pardus);[12,13] domestic cats;[14,15,16,17] captive Owston's palm civets (Chrotogale owstoni);[18] a domestic dog;[19] a free-living stone marten (Martes foina);[20] and a free-living American mink.[21] In these species, the infection resulted in both respiratory and extrarespiratory lesions, demonstrating systemic infection beyond the respiratory system. The most frequently reported clinical signs for all species were respiratory distress, neurologic signs, or both.

The sources of most HPAI virus (H5N1) infections in carnivores were traced to infected birds eaten by the animals.[12,13,14,15,19] Until 2005, carnivores infected with HPAI virus (H5N1) were either wild carnivores kept in captivity or domestic carnivores that ate infected domestic or peridomestic birds.[12,13,14,19] Since 2005, and after the spread of HPAI virus (H5N1) of the Qinghai sublineage (clade 2.2) outside Southeast Asia in poultry and wild bird populations, carnivores infected with HPAI virus (H5N1) included for the first time free-living wild carnivores, which presumably ate infected wild birds.[20,21]

The occurrence of HPAI viruses (H5N1) in wild bird populations is likely to result in the exposure and infection of free-living wild carnivore species. In particular, abundant and widespread species of wild carnivores that have opportunistic feeding habits and that feed on wild birds may be at high risk for exposure. The red fox (Vulpes vulpes) is one of the most abundant and widespread species of wild carnivores in Eurasia. Partly because of rabies eradication,[22,23] fox populations in western Europe have increased drastically since the mid-1980s (e.g., >140% in Germany;[24]). The red fox is also an opportunistic carnivore species and has a diverse diet, which includes small mammals and birds.[24,25] Therefore, it may likely hunt or scavenge wild birds infected with HPAI viruses (H5N1). However, the susceptibility of this species to infection with influenza viruses is unknown.

In this study, we asked 2 questions: 1) Are red foxes susceptible to infection with a wild bird isolate of HPAI virus (H5N1) from clade 2.2? and 2) Can red foxes become infected by the presumed natural route of infection, i.e., after feeding on infected bird carcasses? To answer these questions, we experimentally assessed the excretion pattern (based on route, duration, and concentration of virus excretion) and pathogenicity (based on clinical signs, death rates, and distribution of lesions and virus) of a wild bird isolate of clade 2.2 HPAI virus (H5N1) in red foxes infected intratracheally and in red foxes fed infected bird carcasses.


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