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she was scratched on the right arm by a pet rat while visiting a friend who had several domestic rats ( rattus norvegicus ) .
one rat had been purchased at the end of december 2008 from a pet store .
the rat became sick with sneezing , conjunctival hemorrhages , and epistaxis ; it died 4 days after purchase . on january 4 , 2009 , the patient sought treatment at the emergency department of compigne hospital .
eight days later , the patient was admitted to the hospital with a black necrotic scab on the internal surface of the right arm , regional lymphangitis , and axillar lymphadenopathies ( figure 1 , panel a ) .
after 3 weeks of unsuccessful antimicrobial drug treatment , she underwent surgery to remove the affected area .
cowpox virus infection in 3 persons in northern france caused by transmission from infected pet rats .
cutaneous lesions caused by cowpox virus are shown in patient 1 ( a ) , patient 3 ( b ) and patient 4 ( c , d ) .
panel c was obtained on january 30 , 2009 , panel d on february 6 , 2009 .
negative - staining electron microscopy showed mulberry forms with conspicuous but short , randomly arranged surface tubules ( e ) and capsule forms with deeper stain penetration ( f ) , both highly suggestive of poxvirus .
case - patient 2 was a 17-year - old woman who had purchased a domestic rat at the end of december 2008 .
the rat died within 3 days of purchase and had respiratory symptoms identical to those of the rat that scratched case - patient 1 .
six days after the rat died , an inflammatory cutaneous macular lesion appeared at the base of the patient s neck , causing local pain and intense inflammatory reaction .
amoxicillin - clavulate was prescribed , but the necrotic scab continued to grow , and local pain increased along with fever ( 39c ) ( figure 1 , panel b ) .
she was admitted to the emergency department of compigne hospital on january 14 , 2009 . on january 3 , she had purchased a rat from the same pet store as case - patient 1 . soon afterward , the rat began to cough and show signs of hemorrhagic lachrymal oozing ; the rodent died on january 6 . on january 13 , the patient had maculopapular lesions on the upper right eyelid , on her left shoulder , and at the base of her neck . due to her deteriorating condition
, she was admitted to the emergency department on january 17 with rash characterized by erythema and edema , and painful regional lymphangitis and lymphadenopathy .
case - patient 4 was a 29-year - old woman who reported having been scratched by a rat on january 21 , 2009 .
an inflammatory macule on her clavicle had progressed through papular , vesicular , and pustular stages ; she also had fever and malaise . on january 14 , she had purchased a domestic rat in the same store as the 3 previous case - patients . the rat had respiratory symptoms similar to the previously infected rats and died on january 21 .
the patient was admitted to compigne hospital on january 30 ; examination showed a 20-mm black eschar with a crust , regional lymphangitis , and painful lymphadenopathies ( figure 1 , panels c and d ) .
biopsy specimens of case - patients 13 were sent to the national reference center for rickettsial diseases ( marseille ) on january 21 because anthrax and/or rickettsial disease was suspected .
broad range pcrs were performed for bacteria ( 16s rrna ) ( 7 ) and fungi ( 18s rrna ) ( 8) . in the absence of etiology , and based on information provided by the institut de veille sanitaire , negative - stain electron microscopy was performed on january 26 .
the biopsy samples showed typical poxvirus - like particles ( figure 1 , panels e and f ) .
molecular diagnosis was performed by using pcr targeting a 260-bp fragment in the cowpox hemagglutinin gene ( forward primer 5-tacttttgttactaatatcattag-3 , reverse primer 5-agcagtcaatgatttaattgt-3 ) .
direct sequencing of the pcr product identified cowpox virus by blast analysis ( http://blast.ncbi.nlm.nih.gov/blast.cgi ) against the genbank database .
the virus was isolated by using monolayers of vero cells in 12.5-cm flasks ( 9 ) .
when cytopathic effect was obvious , dna was extracted from the supernatant , and the complete hemagglutinin gene was sequenced from a pcr product ( forward primer 5-ccattggaaaaaacacagtac-3 , reverse primer 5-ccaaatatattcccatagtc-3 ) , amplifying a 1,183-bp region .
electron microscopy and pcr were performed on formalin - fixed scabs from the lesion of case - patient 4 .
both test results were positive morphologically for a poxvirus and by pcr for cowpox virus .
the virus was isolated from serum samples of case - patients 13 and assessed by cytopathic effect on vero cells , electron microscopic morphologic identification , positive pcr amplification , and subsequent direct sequencing .
a 1,047-bp sequence was definitive and used for fine comparative genetic analysis with the full - length hemagglutinin gene sequences available in genbank .
the most closely related sequence corresponded to clone cow ha24 of the catpox 5 isolate of cowpox virus , isolated from a cheetah in 1982 in the united kingdom ( ay902254 ) .
genetic heterogeneity with y902254 comprised 15 mutations ; 10 were nonsynonymous , and 3 were insertions .
phylogenetic analyses indicated that sequences corresponding to these cases grouped together and were clearly distinct from other cowpox virus strains previously reported ( figure 2 ) .
sequence analysis indicated that these 4 infections were caused by a virus strain distinct from other cowpox virus sequences retrieved from genbank .
cpxv , cowpox virus ; ectv , ectromelia virus ; varv , variola virus ; cmlv , camelpox virus ; vacv , vaccinia virus ; hspv , horsepox virus ; mpxv , monkeypox virus .
sporadic human cases of cowpox virus infection have occurred in several european countries over the past few years . for most cases the source was domestic cats ( 46,10,11 ) .
rat - to - human transmission of cowpox virus was described in the netherlands , but the source was a wild rat , not a pet rat ( 12 ) .
we know of only 1 previous case of human cowpox virus infection that may be linked to a pet rat ( 13 ) . in the 4 cases reported here ,
all 4 patients reported scratches caused by rat claws , not bites , while handling the rats as pets . in 3 of the 4 cases , fever ( 39c ) was noticed at the pustular stage , associated with lymphangitis and regional adenopathies .
interviews with the 4 case - patients showed all had purchased or had been in contact with domestic rats originating from the same pet store .
further investigations traced the origin of the cowpox virus - infected rats to a rat breeder in the czech republic ( 14 ) . recently ,
similar human cases linked to contact with pet rats have been reported in france , suggesting that the outbreak may involve more cases than were initially realized ( 14 ) .
the situations in france and germany mimic the monkeypox outbreak in the united states , i.e. , human transmission of the virus by pet prairie dogs contaminated by probable contact with gambian rats imported from africa and directly associated with a us pet retailer ( 15 ) .
our study and the us outbreak emphasize the need for extreme caution when humans adopt animals of exotic origin as pets .
our study justifies the establishment of a national diagnostic capability and the corresponding human expertise to enable rapid diagnosis and identification of human pathogens that can cause unimaginable levels of disease in our communities .
in early 2009 , four human cases of cowpox virus cutaneous infection in northern france , resulting from direct contact with infected pet rats ( rattus norvegicus ) , were studied . 
 pet rats , originating from the same pet store , were shown to be infected by a unique virus strain . 
 infection was then transmitted to humans who purchased or had contact with pet rats .