Linking rattiness, geography and environmental degradation to spillover Leptospira infections in marginalised urban settings: An eco-epidemiological community-based cohort study in Brazil.

Background: Zoonotic spillover from animal reservoirs is responsible for a significant global public health burden, but the processes that promote spillover events are poorly understood in complex urban settings. Endemic transmission of Leptospira, the agent of leptospirosis, in marginalised urban communities occurs through human exposure to an environment contaminated by bacteria shed in the urine of the rat reservoir. However, it is unclear to what extent transmission is driven by variation in the distribution of rats or by the dispersal of bacteria in rainwater runoff and overflow from open sewer systems. Methods: We conducted an eco-epidemiological study in a high-risk community in Salvador, Brazil, by prospectively following a cohort of 1401 residents to ascertain serological evidence for leptospiral infections. A concurrent rat ecology study was used to collect information on the fine-scale spatial distribution of 'rattiness', our proxy for rat abundance and exposure of interest. We developed and applied a novel geostatistical framework for joint spatial modelling of multiple indices of disease reservoir abundance and human infection risk. Results: The estimated infection rate was 51.4 (95%CI 40.4, 64.2) infections per 1000 follow-up events. Infection risk increased with age until 30 years of age and was associated with male gender. Rattiness was positively associated with infection risk for residents across the entire study area, but this effect was stronger in higher elevation areas (OR 3.27 95% CI 1.68, 19.07) than in lower elevation areas (OR 1.14 95% CI 1.05, 1.53). Conclusions: These findings suggest that, while frequent flooding events may disperse bacteria in regions of low elevation, environmental risk in higher elevation areas is more localised and directly driven by the distribution of local rat populations. The modelling framework developed may have broad applications in delineating complex animal-environment-human interactions during zoonotic spillover and identifying opportunities for public health intervention. Funding: This work was supported by the Oswaldo Cruz Foundation and Secretariat of Health Surveillance, Brazilian Ministry of Health, the National Institutes of Health of the United States (grant numbers F31 AI114245, R01 AI052473, U01 AI088752, R01 TW009504 and R25 TW009338); the Wellcome Trust (102330/Z/13/Z), and by the Fundação de Amparo à Pesquisa do Estado da Bahia (FAPESB/JCB0020/2016). MTE was supported by a Medical Research UK doctorate studentship. FBS participated in this study under a FAPESB doctorate scholarship.

A multivariate geostatistical framework for combining multiple indices of abundance for disease vectors and reservoirs: a case study of rattiness in a low-income urban Brazilian community.

A key requirement in studies of endemic vector-borne or zoonotic disease is an estimate of the spatial variation in vector or reservoir host abundance. For many vector species, multiple indices of abundance are available, but current approaches to choosing between or combining these indices do not fully exploit the potential inferential benefits that might accrue from modelling their joint spatial distribution. Here, we develop a class of multivariate generalized linear geostatistical models for multiple indices of abundance. We illustrate this novel methodology with a case study on Norway rats in a low-income urban Brazilian community, where rat abundance is a likely risk factor for human leptospirosis. We combine three indices of rat abundance to draw predictive inferences on a spatially continuous latent process, rattiness, that acts as a proxy for abundance. We show how to explore the association between rattiness and spatially varying environmental factors, evaluate the relative importance of each of the three contributing indices and assess the presence of residual, unexplained spatial variation, and identify rattiness hotspots. The proposed methodology is applicable more generally as a tool for understanding the role of vector or reservoir host abundance in predicting spatial variation in the risk of human disease.

Using fine-scale spatial genetics of Norway rats to improve control efforts and reduce leptospirosis risk in urban slum environments.

The Norway rat (Rattus norvegicus) is a key pest species globally and responsible for seasonal outbreaks of the zoonotic bacterial disease leptospirosis in the tropics. The city of Salvador, Brazil, has seen recent and dramatic increases in human population residing in slums, where conditions foster high rat density and increasing leptospirosis infection rates. Intervention campaigns have been used to drastically reduce rat numbers. In planning these interventions, it is important to define the eradication units - the spatial scale at which rats constitute continuous populations and from where rats are likely recolonizing, post-intervention. To provide this information, we applied spatial genetic analyses to 706 rats collected across Salvador and genotyped at 16 microsatellite loci. We performed spatially explicit analyses and estimated migration levels to identify distinct genetic units and landscape features associated with genetic divergence at different spatial scales, ranging from valleys within a slum community to city-wide analyses. Clear genetic breaks exist between rats not only across Salvador but also between valleys of slums separated by <100 m-well within the dispersal capacity of rats. The genetic data indicate that valleys may be considered separate units and identified high-traffic roads as strong impediments to rat movement. Migration data suggest that most (71-90%) movement is contained within valleys, with no clear source population contributing to migrant rats. We use these data to recommend eradication units and discuss the importance of carrying out individual-based analyses at different spatial scales in urban landscapes.

A Two-Year Ecological Study of Norway Rats (Rattus norvegicus) in a Brazilian Urban Slum.

The Norway or brown rat (Rattus norvegicus) is among the most ubiquitous of rodents. However, the lack of studies describing Norway rat populations from tropical areas have limited our understanding regarding their demography and seasonal dynamics. In this study, we describe seasonal pattern in the abundance, reproductive parameters, and morphometrics of Norway rat populations in Salvador, Brazil. Rodents were trapped over four seasonal trapping periods (2013-2014) from three valleys. A total of 802 Norway rats were trapped over the course of the study over 7653 trap-nights. Norway rat abundance was high, but there was no significant differences between seasons. The reproductive parameters (e.g. frequency of pregnant and lactating females) did not show statistical differences between seasons. Female rats collected in the rainy season were heavier and older than females from the dry season. Salvador rats had a high incidence of pregnancy and birth rate (estimated birth rate of 79 young per year) compared to previous studies. The information generated is critical for the understanding of the ecology of Norway rat, the main reservoir of Leptospira in Salvador. However, future studies examining the effect of rodent control programs aimed at reducing populations, and determining rates of recovery, will further clarify our understanding of population dynamics.

Warming modifies trophic cascades and eutrophication in experimental freshwater communities.

Climate warming is occurring in concert with other anthropogenic changes to ecosystems. However, it is unknown whether and how warming alters the importance of top-down vs. bottom-up control over community productivity and variability. We performed a 16-month factorial experimental manipulation of warming, nutrient enrichment, and predator presence in replicated freshwater pond mesocosms to test their independent and interactive impacts. Warming strengthened trophic cascades from fish to primary producers, and it decreased the impact of eutrophication on the mean and temporal variation of phytoplankton biomass. These impacts varied seasonally, with higher temperatures leading to stronger trophic cascades in winter and weaker algae blooms under eutrophication in summer. Our results suggest that higher temperatures may shift the control of primary production in freshwater ponds toward stronger top-down and weaker bottom-up effects. The dampened temporal variability of algal biomass under eutrophication at higher temperatures suggests that warming may stabilize some ecosystem processes.