Transmission ecology of canine parvovirus in a multi-host, multi-pathogen system

Abstract

Understanding multi-host pathogen maintenance and transmission dynamics is critical for disease control. However, transmission dynamics remain enigmatic largely because they are difficult to observe directly, particularly in wildlife. Here, we investigate the transmission dynamics of canine parvovirus (CPV) using state-space modelling of 20 years of CPV serology data from domestic dogs and African lions in the Serengeti ecosystem. We show that, although vaccination reduces the probability of infection in dogs, and despite indirect enhancement of population seropositivity as a result of vaccine shedding, the vaccination coverage achieved has been insufficient to prevent CPV from becoming widespread. CPV is maintained by the dog population and has become endemic with approximately 3.5-year cycles and prevalence reaching approximately 80%. While the estimated prevalence in lions is lower, peaks of infection consistently follow those in dogs. Dogs exposed to CPV are also more likely to become infected with a second multi-host pathogen, canine distemper virus. However, vaccination can weaken this coupling, raising questions about the value of monovalent versus polyvalent vaccines against these two pathogens. Our findings highlight the need to consider both pathogen- and host-level community interactions when seeking to understand the dynamics of multi-host pathogens and their implications for conservation, disease surveillance and control programmes.

Keywords: coinfection; domestic–wildlife interface; longitudinal serology; maintenance host; state–space models; vaccine shedding.

Figure 1.

Data used in this study. (a) Sampling locations of domestic dogs (grey circles) and lions (blue circles) in the Serengeti ecosystem. The Serengeti National Park (SNP) is shown in the dark grey shaded area. (b) Observed annual seroprevalence of CPV in domestic dogs (grey) and African lions (blue), and of CDV (green) in dogs. The orange line corresponds to the regional vaccination coverage. Sample sizes available in electronic supplementary material, table S1.

Figure 2.

Estimated CPV temporal profiles. (a) Mean annual probability of CPV natural infection (grey) and vaccine-shed (red) seropositivity in domestic dogs, and village vaccination coverage (orange dashed line). (b) Mean annual probability of CPV infection in lions. Associated 50%, 75% and 95% credible intervals shown in increasingly lighter colour shading. Vertical dashed line corresponds to year 2003, the start of larger vaccination efforts.

Figure 3.

Effects of vaccination. (a) Posterior distribution of the parameter describing the influence of shedding (φ in equation (2.1)). (b) Mean difference between the estimated prediction of the annual probability of CPV infection and that without the vaccination effect (black). This difference is negative if vaccination reduces the probability of CPV infection. Associated 50%, 75% and 95% credible intervals shown in increasingly lighter shading. Annual village vaccination coverage shown in orange. Inset, the posterior distribution of the parameter describing the influence of vaccination on the annual probability of dog infection (v₁). (Online version in colour.)

Figure 4.

Cross-species transmission of CPV. Posterior distributions of the parameters describing the influence of the probability of infection of dogs on that of lions (Ω_DL; grey) and vice versa (Ω_LD; blue). (Online version in colour.)

Figure 5.

Co-exposure patterns. (a) Venn diagram representing the observed number of dogs exposed to CPV (light grey) and CDV only (intermediate grey) and co-exposed with both diseases (dark grey). (b) Posterior distributions of the parameters describing the influence of CPV (dotted line) and CDV (dashed line) only, and that of both diseases if they are independent (p_CPV × p_CDV; solid line) on the co-exposure (p_both) dynamics. (Online version in colour.)

Figure 6.

Influence of CPV and CDV on co-exposure. Difference between the predicted annual probability of being co-exposed to CPV and CDV, and that without the effect of CDV (dotted line) and CPV (dashed line). This difference is negative if shutting down the effect of one pathogen reduces the probability of co-exposure. Shaded area corresponds to the back-predicted period.