1. generally, groups of dogs with a high percentage of seroconversion will have the highest probability of surviving challenge;
2. on an individual basis:

• a dog with neutralising antibodies just before challenge will have the best chance of surviving a severe challenge;
• a dog with no detectable neutralising antibodies just before challenge will have a high chance of surviving a severe challenge if it seroconverted after vaccination;
• some dogs will not survive a severe challenge even if they have detectable neutralising antibody titres before challenge; generally these titres are the lowest of the group.

• inappropriate vaccination with inadequately stored or improperly injected vaccine
• vaccination during the incubation of rabies or before the onset of an immunological response
• a heavy challenge overwhelming host defences
• intrinsic incapacity in the host.

Whatever the origins of rabies cases recorded in vaccinated dogs, their number seems relatively low in areas contaminated with fox rabies (e.g. in Europe) (20). In France, only ten cases of so-called vaccination failures in dogs (and four among cats) have been registered over a period of twenty-three years (6). This number should be compared with the 4,250,000 cats and dogs vaccinated annually in France (this figure is based on the annual number of vaccine doses sold for domestic carnivores). The probability of a cat or dog becoming rabid if vaccinated can be estimated as 14/(23 x 4,250,000), which is less than 1/6,980,000. In France, dogs in contact with a rabid animal in an enzootic area are not sacrificed and can be kept alive if, prior to contamination, they have been properly vaccinated (with certificate and identification). In such cases, the animals are immediately revaccinated. A study of more than 3,500 dogs which had close contacts (bites in 36% of cases) with foxes (mainly) or other carnivores which were diagnosed as rabid by laboratory examination, revealed that only three dogs developed rabies (50). The failure rate in animals which were definitely contaminated can be estimated as 3/3,500, given that injection of vaccine after contamination has been shown to provide no protection (20). It must be emphasised that these failures were recorded before 1984 and that failure is now less probable, given the generalisation of adjuvanted vaccines for dogs. In the United States of America, four rabies vaccine failures were recorded in cats and dogs in 1988 with 33,182,575 vaccinated domestic carnivores the same year (rate = 1/8,296,000) (34).

Such evaluations could be useful in comparing the risks of vaccination with those of quarantine. For even when they are strictly managed, quarantines still entail a risk. For instance, in many countries, the quarantine period is six months. However, longer incubation periods have been reported in dogs (8.5 months after challenge) (67) and in other carnivores (12 months or more for foxes) (57). According to Sasaki and colleagues (55), Beynon determined that a quarantine period of nine months would be necessary to detect all cases of incubating rabies with a 95% degree of confidence.

3. STUDIES IN CATS

3.1. Neutralising antibodies after vaccination

Although fewer studies have been conducted on vaccination of cats against rabies, several of the characteristics observed in dogs were also observed in cats:

• the kinetics of neutralising antibodies follow the same profile in the two species (8, 23, 64)
• the relationship between the potency of vaccines and the level of neutralising antibodies: Lawson and colleagues (44) have shown that the less diluted modified live vaccines induced the highest rate of seroconversion in vaccinated cats (Table 9), but Lazarowicz and colleagues (45) obtained no correlation of the antigenic value of inactivated virus vaccines as determined by the NIH test and mean neutralising antibody titres in vaccinated cats. However, as for dogs, it is necessary to take account of the fact that the production of antibodies (and protection against challenge) obtained after administration of live virus vaccine (44) and inactivated virus vaccine (45) can show great divergence and are not readily comparable.
• intramuscular vaccination provides longer lasting protection than subcutaneous vaccination (Table 10) (59).

Table 9

Laboratory cats: intramuscular vaccination with various vaccines, challenge with rabies virus fox strain five weeks and four years after vaccination (44)

ERA: Elizabeth (Gaynor) Rokitniki Abelseth
HEP: high egg passage

Concerning the influence of age, Précausta and colleagues (53) described the good neutralising antibody response achieved by three-month-old kittens, even those born of immune queens.

To our knowledge, Blancou and colleagues (18, 19) are the only authors who have tested vaccination results on owned cat populations. Pet cats appeared to respond well to the administration of an adjuvanted vaccine. In contrast, the same authors obtained mild or zero neutralising antibody responses when vaccinating cats sampled from stray populations in France. With stray cats, the worst result was obtained with non-adjuvanted vaccines: 5 of 9 individuals did not respond (Fig. 7).

Fig. 7

Influence of the breeding standards of cats on the level of rabies antibody reached one year after vaccination

Comparison of laboratory cats, pet cats in France and stray cats in Tunisia (19)

3.2. Level of neutralising antibodies and result of challenge

Challenge under laboratory conditions

Although there are few field studies on the immunity of pet or stray cat populations, there are numerous laboratory studies on challenge of vaccinated cats (Tables 10 to 12).

Table 10

Laboratory cats: intramuscular vaccination with tissue culture adjuvanted vaccine, challenge with rabies virus NYC-Ga strain, one to three years after vaccination (59)

* Prior to challenge the cat which died of rabies had an antibody titre of 1/2 (endpoint neutralising dilution)

Table 11

Laboratory cats: subcutaneous vaccination with tissue culture vaccine, challenge with rabies virus NYC-Ga strain, 3.4 to 3.7 years after vaccination (64)

Table 12

Laboratory cats: challenged with rabies virus NYC-Ga strain four to six-and-a-half months after vaccination (42)

* Measured by the NIH test, expressed in IU/dose
** The cat which died of rabies had a pre-challenge titre of 5.34 IU/ml
*** The cats which died of rabies had the lowest antibody titres
ERA: Elizabeth (Gaynor) Rokitniki Abelseth

Challenge was performed with a dog strain (NYC-Ga) mimicking the situation of canine street rabies (42, 61, 64) or, in other experiments, a fox strain mimicking the situation of sylvatic fox rabies in continental Europe (38, 44). With both strains, the general conclusion was the same as for dogs: the probability of a cat surviving challenge can be predicted by the level of neutralising antibodies. Of course, unexpected deaths can occur: Kihm and colleagues (42) reported a rabies death in a cat which had a pre-challenge titre of 5.34 IU, and Blancou and colleagues (18) in another cat with a pre-challenge titre of 0.87 IU/ml.

The cumulative challenge results on cats reported by Bunn (26, 27) are described in Figure 8 and Tables 13 and 14. With a neutralising antibody level of more than 0.1 IU (measured by MNT) or more than 0.2 IU (measured by RFFIT), all of the cats survived challenge.

Fig. 8

Survival rate after challenge of laboratory cats correlated with the level of rabies antibody reached before challenge

Cats were vaccinated with various vaccines and challenged one year after vaccination with NYC-Ga, fox or skunk strains; the number of cats in each class is written at the top of the bars (27)

Table 13

Challenge results from rabies immonogenicity tests conducted in dogs and cats with vaccines approved for use in the United States of America (27)

* antibody titres expressed as 50% endpoint neutralising dilutions established by either the MNT or RFFIT
** challenge results are expressed as number of animals which died/number of animals challenged
SAD: Street Alabama Dufferin strain

Table 14

Neutralising antibody titres in dogs and cats and protection from challenge with rabies virus (26)

* antibody titres expressed as 50% endpoint dilutions established by either the virus neutralisation test in mice (MNT) or the rapid fluorescent focus inhibition test (RFFIT)

** challenge results are expressed as number of animals which died/number of animals challenged

Natural infection of vaccinated cats

The safety problem associated with the receptivity of cats to live virus vaccines such as Flury LEP and HEP or Street Alabama Dufferin (SAD) strain vaccines will not be reviewed here (11). But it should be remembered that while cats are the species with the largest number of rabies cases directly induced by the inoculation of live modified virus strains, other species such as dogs and foxes are also receptive (72).

Inactivated virus vaccines are employed on cats as they are more efficient in protecting the species against natural challenge. However, considering the results of challenge experiments on vaccinated cats, natural infection among vaccinated pet cats is suspected to be as frequent as for vaccinated dogs. But investigations on rabies cases in vaccinated cats are scarce: apart from the four cases reported in France (6) there appear to be no other reports. This discrepancy is due to the fact that dogs have been studied considerably more than cats.

4. THE SIGNIFICANCE OF NEUTRALISING ANTIBODIES IN NON-VACCINATED CARNIVORES

4.1. Non-specific and specific neutralising factors

Sekine and colleagues (58) found that sera of normal rabbits and guinea-pigs contained non-specific inhibitors capable of neutralising the virus in the presence of complement. In a well-conducted seroneutralisation on mice, therefore, inactivation of sera is performed for 30 minutes at 56°C. Virus inhibition by other substances was described in infected skunks and foxes (74). Infection by mycobacteria, e.g. Bacillus Calmette-Guérin (BCG), can also induce the production of rabies neutralising antibodies in mice and provide protection against rabies in a number of animals (70). Since more specific immunological tests (such as enzyme-linked immunorescent assay: ELISA) have become widespread, non-specific neutralising factors have not generated further scientific reports.

In endemic areas, serosurveys in wild carnivores demonstrated a high proportion of apparently healthy individuals with neutralising antibodies in serum (54, 71) and it has been suggested that these antibodies may have been produced following contact with virus from other species, which was therefore immunising but rarely fatal (12). However, the same observations have also been reported for dog populations in areas where dog rabies is endemic: in Thailand, in areas where no canine vaccination programme has ever been conducted, 15-20% of dogs had neutralising antibodies, yet remained perfectly normal when observed for prolonged periods (75); similar results had also been reported previously in other countries of Asia and in Africa (3, 36). These observations correlate with the high probability of inter-individual contamination within the reservoir species, which is not the case for pet populations in areas where rabies is endemic. The possibility of non-fatal contamination of dogs by non-canine strains (e.g. those from wild animals living in the region) has also been proposed (20). Several questions thus arise regarding:

1. the specificity of serum titrations and the threshold level for protection against rabies;
2. the possibility of rabies outbreaks in naturally seroconverted dogs, and the interval between seroconversion and the onset of clinical symptoms.

4.2. Rabies infections

The viral infection triggers the production of neutralising antibodies. When a high dose of rabies virus reaches the central nervous system, neutralising antibodies are not detectable before or at the onset of clinical signs; they are usually induced by longer incubation periods. This phenomenon has been studied mainly in laboratory rodents, which supply the chief model of rabies immunopathology (49, 73). Unfortunately (but not surprisingly, considering the difficulty of handling rabid carnivores), there appears to be no literature on the frequency and intensity of neutralising antibody production in non-vaccinated infected cats and dogs. Some data can be found in articles by Artois and colleagues (4), Blancou and colleagues (17) and Fekadu (36) regarding latent or abortive rabies.

Bell and colleagues (10) proved that dogs which recovered from rabies after intracerebral inoculation of homologous strains, had high titres of neutralising antibody in the cerebrospinal fluid as well as in serum and retained these titres for several months, whereas vaccinated dogs did not have high cerebrospinal fluid titres. Murphy and colleagues (48) demonstrated the same phenomenon in cats.

Bell and colleagues (9) were the first to apply cerebrospinal fluid titration for an epidemiological survey. Of 120 dogs sampled in an area where rabies was enzootic (Buenos Aires), none was found to be positive; thus, it cannot be concluded that non-fatal rabies is common.

Blenden and colleagues (21) have suggested that the kinetics of antibody levels in blood and cerebrospinal fluid should be compared, to determine whether specific antibodies have been produced by infection or by immunisation. Without a booster after a first blood and cerebrospinal sampling, the antibody level should remain stable in cases of immunisation, or increase in cases of infection. In fact, such procedures have never been routinely used anywhere. Indeed, given the variability of the titration test, the constancy of an antibody titre over time is difficult to verify even in a vaccinated animal.

Given the lack of easily-performed experimental methods, the only basis for considering that an individual dog or cat possessing rabies neutralising antibodies has been vaccinated is good individual identification and certification.

5. DISCUSSION

Laboratory conditions described in the challenge of vaccinated cats and dogs generally appear more severe than natural conditions of challenge in the field. In normal practice, experimenters use extremely long intervals between vaccination and challenge (three to five years) and high virus doses involving 100% mortality in controls. In areas contaminated by fox rabies, natural challenge is not as severe for dogs and this could compensate for the fact that the health status of pets may be lower than that of dogs bred in the laboratory. Epidemiological observation is by far the more important evidence; in continental Europe, rabies vaccination of cats and dogs is so efficient that where the annual risk of a fatal case of rabies has been evaluated for a vaccinated pet, this risk is minute (1/6,980,000). It is also noteworthy that in continental Europe, fox rabies has never been propagated by domestic animals from an enzootic area to a free one - even if administrative rules concerning compulsory confinment, leashing or vaccination have sometimes been broken either deliberately or by the simple fact that rabid pets have escaped from their owners.

If a neutralising antibody titration were required for certifying the immunological capacity of vaccinated animals, two questions would arise regarding:

1. the choice of techniques for antibody titration
2. the definition and acceptance of a minimum antibody titre considered as providing protection against rabies.

A general analysis of challenge experiments leads to the conclusion that neutralising antibody titres enable prediction of survival more often on a qualitative basis (i.e. Do the animals have detectable neutralising antibodies or not?) than on a quantitative basis. This fact becomes apparent when one tries to determine a "protective" threshold. For this purpose, either method of seroneutralisation (RFFIT or MNT) can be employed, provided a correlation between the two methods has been demonstrated in the same laboratory (14, 66).

Agreements on the international transfer of dogs and cats could be formulated, therefore, based on a designated minimum level of neutralising antibodies, and could be proposed as an alternative to quarantine measures. The designated threshold could be based on the results presented in this study. The security of the protection constituted by this threshold would be increased by the extent to which it excedes the level recognised as effective against experimental challenge in cats and dogs (0.1 IU/ml and 0.2 IU/ml, respectively, measured by RFFIT).

6. ACKNOWLEDGEMENT

The author wishes to express his gratitude to Dr J. Blancou for kindly revising the manuscript of this paper.

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I would like to express my sincere gratitude to Peter and Kris Christine in allowing me to share this information with all visitors to my site.

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