Canine vector-borne infections in Mauritius
The dogs that were tested during this study were free-roaming strays collected throughout
the island of Mauritius and kept at the MSAW pound in Port-Louis. Since it took several
days to collect all the samples, new batches of dogs were continuously arriving to
be assessed. In this regard therefore, the results likely provide a representative
snapshot of several canine vector-borne diseases amongst the stray population throughout
this southern Indian Ocean island. However, it should be noted that this stray population
was unlikely to be receiving ectoparasiticide prophylaxis and may therefore not be
representative of the entire canine population on the island.
Not unexpectedly, given the environmental conditions and the hosts sampled, the majority
of the ticks (98%) were R. sanguineus, the brown dog tick. Rhipicephalus sanguineus is the most widespread tick in the world and has been previously documented as being
the most common tick found on dogs in Mauritius 1],7],8]. Rhipicephalus sanguineus is the main vector for E. canis, the cause of canine monocytic ehrlichiosis (CME), and is also responsible for the
transmission of other pathogens to dogs including Babesia canis vogeli, Hepatozoon canis, and possibly Anaplasma platys9]. In addition, in other parts of the world, R. sanguineus has been implicated as a vector for pathogens of human medical importance, notably
Mediterranean fever (Rickettsia conorii) and other rickettsial infections (Rickettsia massiliae and Rickettsia rickettsia) 7],10]. The brown dog tick also serves as an intermediate host for the dog filarial parasites
Cercopithifilaria bainae and Cercopithifilaria grassii, which were not tested for in this study 10],11].
Interestingly, three A. variegatum ticks were collected from a single dog. This tick is most commonly associated with
cattle in Africa but has been known to feed on other animal species including dogs
and people 1],12],13]. Amblyomma variegatum is widely distributed throughout Africa and has been reported previously in Mauritius,
predominantly on cattle and deer 1],14],15]. Our results suggest that this tick is not commonly found in the Mauritian dog population;
it is possible the dog was previously in contact with cattle or deer prior to being
captured and taken to the shelter, but this was not possible to verify. Amblyomma variegatum is the principal vector responsible for the spread of cowdriosis (Ehrlichia ruminantium) in tropical Africa and is also a vector for Rickettsia africae and Babesia divergens, both of which are potential human pathogens 1],13]. The relevance of A. variegatum in relation to canine vector-borne disease is unclear: that particular dog was also
parasitised by R. sanguineus and was positive for canine ehrlichiosis.
With the widespread presence of R. sanguineus ticks throughout the dog population, it was not surprising to find approximately
one third of the dogs tested had antibodies to Ehrlichia spp. Ehrlichia canis has not previously been documented in Mauritius, although there is clinical suspicion
amongst veterinarians and anecdotal evidence of its presence in the island (Ignace,
unpublished observations) 2]. Canine monocytic ehrlichiosis results in a multi-systemic disease in dogs with clinical
signs that range from mild to life-threatening (e.g. terminal myelosuppressive CME)
16]. The relatively high prevalence of ehrlichial infection in the study population should
alert veterinarians to the likely importance of the disease with regards to canine
health in Mauritius. The diagnostic test used in this study (Snap 4Dx Plus, IDEXX
laboratories, Westbrook, ME, USA) does not differentiate between E. canis and Ehrlichia ewingii, and unfortunately we were unable to investigate this further by molecular testing.
Ehrlichia ewingii is believed to be transmitted by Amblyomma americanum in the southern USA and the lone star tick has never been documented in Mauritius
17]. However, there are reports of E. ewingii in Cameroon and Brazil, which are other regions not known to be enzootic for A. americanum18],19], potentially suggesting a different vector for this pathogen and we are therefore
unable to confidently exclude its presence in Mauritius.
Approximately 15% of the dogs were seropositive for antibodies to Anaplasma, which could either represent Anaplasma phagocytophilum or Anaplasma platys infections (Snap 4Dx Plus, IDEXX laboratories, Westbrook, ME, USA). Anaplasma phagocytophilum is the cause of granulocytic anaplasmosis, infecting neutrophils of the canine host,
and manifests clinically as non-specific signs of disease such as lameness, lethargy,
pyrexia 20]. This member of the Anaplasmataceae is transmitted by Ixodes spp. ticks, which have not been previously identified on dogs in Mauritius, and their
northern hemisphere distribution makes this form of anaplasmosis unlikely to occur
in the island. A more plausible explanation for these results is infection by A. platys21]. Anaplasma platys causes canine infectious cyclic thrombocytopenia (CICT) and may further complicate
the pathogenesis of E. canis; both pathogens are generally found in similar geographical locations, both are transmitted
by the same tick species, and it is common to find dogs concurrently infected with
both pathogens (5% of the dogs in our study were infected with both A. platys and E. canis) 21].
Borrelia burgdorferi, the causative agent of Lyme disease, is transmitted by Ixodes spp. ticks. Clinical signs in dogs include lameness from inflammation of joints,
lethargy and loss of appetite 22]. To the best of our knowledge autochthonous cases of Lyme disease have never been
documented in Mauritius and with the presumed absence of the documented Ixodes spp. vectors, it is not believed to be present in the island. None of the dogs tested
in this study returned a positive antibody test to the C6 antigen, a specific and
highly conserved antigen expressed by members of the Borrelia burgdorferi genogroup sensu lato.
Hepatozoonosis in dogs is caused by two species; H. americanum and H. canis. To date, H. americanum has only been found in the United States and is transmitted by Amblyomma maculatum in that country. H. canis causes a much milder disease (anaemia, lethargy and often subclinical) and is transmitted
by R. sanguineus throughout the world 23],24]. Despite causing mild disease, H. canis was found to be associated with lower PCV values in our dog population (p=0.03).
This may be explained by the fact that only two dogs had single infections with H. canis, and that lower PCV values may actually be due to co-infections with other pathogens.
Hepatozoonosis is more difficult to diagnose as serological testing is not readily
available for the causative pathogen, and either blood smears or PCR are required
instead for diagnosis. The white cells were able to be visualised clearly by microscopy
and H. canis gamonts were seen within the neutrophils of nine dogs. This is the first record of
canine Hepatozoon infection in Mauritius.
Dirofilaria immitis is the cause of heartworm disease and is transmitted by mosquitoes. It has a worldwide
distribution. Clinical signs include coughing, lethargy and exercise intolerance but
some dogs have subclinical disease. The test used in this study detects D. immitis antigen from mature female worms only, therefore, a positive result indicates infection
with at least one mature female heartworm (6Â months old) 21]. Interestingly 7 out of the 14 antigen positive dogs (50%; 95% CI 23, 77) were amicrofilaraemic
on examination of blood smears, indicating the presence of occult infections in these
dogs 25]. High percentages of occult infections are not uncommon in endemic areas and have
previously been reported in central Portugal 26],27]; such infections have obvious diagnostic implications as clinicians must be careful
when ruling out heartworm disease on the basis of microscopic work alone. Regardless,
visualising microfilariae in blood smears is an insensitive way of quantifying the
disease burden and should not be used as a singular method of diagnosis.
Curiously, one of the dogs was negative for the D. immitis antigen, but had visible microfilariae on microscopic examination. This may be explained
by a false negative serological result (sensitivity of 99.0%- SNAP 4Dx Plus, IDEXX
laboratories, Westbrook, ME, USA), or the dog was infected with a different filarial
organism. Other filarial organisms that could present with microfilariae include,
and are not limited to, Dirofilaria repens, Acanthocheilonema reconditum, Acanthocheilonema dracunculoides, Brugia malayi, Brugia pahangi28]. Results from Chi-square testing also revealed a statistically significant relationship
between lower tick burdens and infection with D. immitis infection. This could be coincidental or may reflect the fact that the dogs came
from various parts of the island where mosquitoes with heartworm may be more prevalent
in areas where ticks are less numerous.
A previous study carried out by Gaunt et al. showed that dogs co-infected with both E. canis and A. platys had more severe anaemia and thrombocytopenia, and a more persistent A. platys infection with a stronger immune response 29]. In our study, the number of pathogens the dogs were infected with did not have any
statistically significant effect on PCV values, indicating that co-infected dogs did
not show greater levels of anaemia. However, it must be acknowledged that PCV is not
necessarily a reliable indicator of the degree of pathology for the vector-borne diseases
we tested for, and that thrombocyte count may be more useful, but this would have
required more sophisticated equipment. Furthermore, the unavailability of molecular
analysis of the blood samples, such as by PCR, is acknowledged as a limitation of
this diagnostic study, and this deficit should be addressed in any future studies
of CVBD on Mauritius.
The relationship between tick burdens and infection rates was also assessed. Studies
have shown that high tick burdens do not correlate with mortality or infection from
tick-borne disease because not all ticks harbour pathogens 30],31]. This, however, was not the case with our study: our results showed that higher tick
burdens were associated with E. canis and H. canis infections, as well as higher co-infection rates. This appears to be logical, as
the more ticks a dog is infected with, the higher the chances of it contracting vector-borne
pathogens.