We report wide variation in patterns of exposure to anthrax and deaths among wild and domestic animal species and populations of the Serengeti ecosystem. Serologic data also highlight the potential value of domestic dogs as indicator species for identifying high-risk areas of infection for livestock and human populations.
The QuickELISA Anthrax-PA kit was a convenient method for assessing seroprevalence in the multiple species examined in this study. The assay does not rely on species-specific or protein A/G conjugates to detect anthrax-specific antibodies and thus can detect any multivalent antibody in a sample. Previous studies that examined antibodies against anthrax in wildlife required unique conjugates specific for each species studied, which necessarily limited the number of species that could be examined (10
). In our study, antibodies were measured in 6 species by using 1 assay. Thus, relative amounts of antibody present in each sample could be directly compared.
Lack of obvious clinical signs before death, inaccessibility of remote locations, decomposition, and hazardous carcasses all affect the quality of anthrax surveillance based on case detection. Despite concerted efforts to obtain samples from suspected cases, we recovered little diagnostic material for confirmation. However, more probable cases were identified on the basis of the appearance of carcasses. Laboratory results may not be conclusive even when diagnostic material is obtained. For example, when multiple blood slides were prepared from 1 buffalo carcass and tested blindly, the results were not consistently positive (only 2 of 6 slides were positive). Some outbreaks are likely to be missed even when probable case detection is used. This suggestion was confirmed by using serosurveillance data; in some agropastoralist areas where anthrax had not been reported, serologic analysis of domestic dogs indicated that the disease had been present.
In contrast to sampling of suspected carcasses, serosurveillance of living animals poses no risk for anthrax infection and therefore offers an opportunity for gaining a better understanding of anthrax epidemiology, particularly in relation to patterns of infection and risk factors for exposure, susceptibility, and death. Our serologic data highlight differences between species in exposure and death, which may be explained by behavior and ecology. However, we caution that although our study suggests great potential for the use of this assay for multiple species comparisons, validation of serologic responses across a range of vaccinated species (possibly using zoo collections) would provide more definitive verification of this proposition and should be prioritized.
Low mortality rates, combined with high seroprevalence rates (always >50% and approaching 90% in Serengeti populations), suggests that wild carnivores are regularly exposed to anthrax without apparent deaths. Although high mortality rates were reported for Kruger lions after periods of low anthrax incidence (4,10
), high seroprevalence rates and low mortality rates are more commonly observed, which suggests a protective immune response presumably associated with more frequent exposure (4,10
). Lions and hyenas may be exposed through consumption of infected prey, but domestic dogs may also be exposed when they scavenge infected carcasses (wildlife and livestock). Low seroprevalence rates and high mortality rates have been reported for cheetahs (15,16
). These rates are consistent with the fact that cheetahs do not scavenge, and solitary hunting exposes them to fewer carcasses than group-hunting lions and hyenas. Although data from this study are limited, detection of probable anthrax cases in cheetah and serval is consistent with a higher susceptibility in these carnivore species.
Relatively lower seroprevalence rates and higher mortality rates for ungulates than for carnivores suggest less routine exposure, higher susceptibility, or both. Major differences in herbivore susceptibility are inferred from the wide variation in seroprevalence detected in species sharing the same grazing areas, and thus probable exposure patterns. Zebras appear to be highly susceptible; however, buffalo and wildebeest can clearly survive infection. Seroprevalence in buffalo was high (≈50%) compared with previous reports for herbivores (≈7%) (10,17
). Comparing seroprevalence in more species would enable assessment of relative roles of exposure versus susceptibility in explaining variable species mortality patterns characteristic for anthrax.
The reported species differences have potential implications for serosurveillance. Among wildlife, carnivores are likely to be the most sensitive indicators of whether infection is present in an area, acting as bioaccumulators of infection through consumption of infected carcasses (18
). However, because lions and hyenas seroconvert at a relatively young age, temporal patterns of exposure from age seroprevalence data are difficult to detect. Furthermore, hyenas are highly mobile in the Serengeti ecosystem (19
), which reduces their utility for identifying specific high-risk areas. However, more detailed investigations of titer levels in relation to timing and location of anthrax outbreaks, including longitudinal studies of serial titers from known animals, could shed light on immunologic responses and enable more information to be obtained from serologic data.
These data suggest a possible utility of serosurveillance in buffalo, whose potential as indicator species has not been explored. Because ≈50% of Serengeti buffalo are seropositive for anthrax, these populations appear to provide a relatively sensitive indicator of the presence and prevalence of anthrax infection, e.g., major differences between populations in SNP and Ngorongoro Crater. Although serologic analysis of wildebeest detected these differences, seroprevalence in wildebeest was lower overall, and the wide-ranging migratory movements of the Serengeti herds limit the utility of these data for detecting spatial patterns. In comparison, buffalo herds range over relatively restricted areas, and serologic data can pinpoint high-risk areas. In many protected areas of Africa, buffalo are already routinely sampled for surveillance of diseases, such as rinderpest, bovine tuberculosis, and foot-and-mouth disease. We suggest that in areas where buffalo surveillance is ongoing, there is added value in using serum samples for monitoring anthrax exposure patterns. Serologic analysis of buffalo and analysis of environmental risk factors could also assist wildlife management strategies, e.g., risks associated with reintroductions of rhinoceros in different areas of the Serengeti, and identify priority areas for enhanced risk-based surveillance.
Domestic dogs have high potential value as indicators of human and livestock diseases (1,18
). They are regularly exposed to a wide range of infections in disease-endemic areas; they are abundant and widely distributed, especially in developing countries; they are generally accessible for safe handling and sampling; they can be sampled at young ages, which enables reasonably accurate timing of outbreaks; and they live in close association with humans and livestock, which makes them good indicators of risk. In addition, vaccination campaigns present a cost-effective opportunity for obtaining large numbers of domestic dog samples (18
). Consistent with these expectations, we have demonstrated that dogs in the Serengeti can be useful indicators of anthrax. They can be used to detect infection in an area, even when anthrax is not identified in other species; they reflect differences in infection prevalence in different areas; they can provide information about the timing of outbreaks (we observed variation in exposure with age) (); and they serve as an indicator of livestock and human disease risk and provide a basis for risk-based surveillance and targeted implementation of prevention measures (e.g., livestock vaccination or public health campaigns).
In conclusion, we demonstrated that serologic investigations of wildlife and domestic animals can provide valuable information about patterns of anthrax transmission and for identifying areas for risk-based surveillance. Serologic approaches also enable retrospective identification of infected areas and timing of outbreaks where case surveillance is limited because of remoteness of an area, poor reporting of cases to local or central authorities, misdiagnosis, and difficulties in performing confirmatory laboratory diagnostic tests. Further research may enable more effective use of serologic data if insights can be gained into how antibody levels relate to timing and degree of exposure.