Impact of Environment and Social Gradient on Leptospira Infection in Urban Slums

Leptospirosis, a life-threatening zoonotic disease, has become an important urban slum health problem. Epidemics of leptospirosis now occur in cities throughout the developing world, as the growth of slum settlements has produced conditions for rat-borne transmission of this disease. In this prevalence survey of more than 3,000 residents from a favela slum community in Brazil, Geographical Information System (GIS) and modeling approaches identified specific deficiencies in the sanitation infrastructure of slum environments—open sewers, refuse, and inadequate floodwater drainage—that serve as sources for Leptospira transmission. In addition to the environmental attributes of the slum environment, low socioeconomic status was found to independently contribute to the risk of infection. These findings indicate that effective prevention of leptospirosis will need to address the social factors that produce unequal health outcomes among slum residents, in addition to improving sanitation

Influence of Household Rat Infestation on <i>Leptospira</i> Transmission in the Urban Slum Environment

<div><p>Background</p><p>The Norway rat (<i>Rattus norvegicus</i>) is the principal reservoir for leptospirosis in many urban settings. Few studies have identified markers for rat infestation in slum environments while none have evaluated the association between household rat infestation and <i>Leptospira</i> infection in humans or the use of infestation markers as a predictive model to stratify risk for leptospirosis.</p><p>Methodology/Principal Findings</p><p>We enrolled a cohort of 2,003 urban slum residents from Salvador, Brazil in 2004, and followed the cohort during four annual serosurveys to identify serologic evidence for <i>Leptospira</i> infection. In 2007, we performed rodent infestation and environmental surveys of 80 case households, in which resided at least one individual with <i>Leptospira</i> infection, and 109 control households. In the case-control study, signs of rodent infestation were identified in 78% and 42% of the households, respectively. Regression modeling identified the presence of <i>R. norvegicus</i> feces (OR, 4.95; 95% CI, 2.13–11.47), rodent burrows (2.80; 1.06–7.36), access to water (2.79; 1.28–6.09), and un-plastered walls (2.71; 1.21–6.04) as independent risk factors associated with <i>Leptospira</i> infection in a household. We developed a predictive model for infection, based on assigning scores to each of the rodent infestation risk factors. Receiver operating characteristic curve analysis found that the prediction score produced a good/excellent fit based on an area under the curve of 0.78 (0.71–0.84).</p><p>Conclusions/Significance</p><p>Our study found that a high proportion of slum households were infested with <i>R. norvegicus</i> and that rat infestation was significantly associated with the risk of <i>Leptospira</i> infection, indicating that high level transmission occurs among slum households. We developed an easily applicable prediction score based on rat infestation markers, which identified households with highest infection risk. The use of the prediction score in community-based screening may therefore be an effective risk stratification strategy for targeting control measures in slum settings of high leptospirosis transmission.</p></div

Logistic regression analysis of rodent-related and environmental characteristics associated with <i>Leptospira</i> transmission and scoring system at household level.

a<p>Odds ratios (OR) and 95% confidence intervals (CI) are shown for analyses. Logistic regression was performed to obtain estimates for odds ratios which were adjusted for covariates in the final model.</p>b<p>Assignment of points to risk factors was based on a linear transformation of the corresponding <i>β</i> regression coefficient. The coefficient of each variable was divided by 0.90 (the lowest <i>β</i> value, corresponding to Un-plastered walls), multiplied by two, and rounded to the nearest integer.</p>c<p>Walls composed of exposed bricks without external application of stucco or plastering.</p><p>Logistic regression analysis of rodent-related and environmental characteristics associated with <i>Leptospira</i> transmission and scoring system at household level.</p

Receiver operating characteristic (ROC) curve for based logistic regression model score system.

<p>AUC (area under the curve) was 0.78 (95% CI 0.71–0.84).</p

Rodent-related and environmental characteristics associated with <i>Leptospira</i> transmission among case and control households at the community study site, Salvador, Brazil.

a<p>Case and control households comprised of households in which cohort subject(s) with evidence of <i>Leptospira</i> infection resided and neighborhood households which were located >30 m of a case household and did not have a member with evidence of <i>Leptospira</i> infection during the study period, respectively.</p>b<p>Median and inter-quartile range (IQR) values are shown for continuous variables.</p>c<p>Values are not shown for non-significant associations.</p>d<p>Categories and variable defined in the CDC form <a href="http://www.plosntds.org/article/info:doi/10.1371/journal.pntd.0003338#pntd.0003338-CDC1" target="_blank">[22]</a>.</p>e<p>Presence of exposed earth slope (>45°) within 10 m of the household.</p>f<p>Walls composed of exposed bricks without external application of stucco or plastering.</p><p>Rodent-related and environmental characteristics associated with <i>Leptospira</i> transmission among case and control households at the community study site, Salvador, Brazil.</p

Environmental variables related to source of food, water, harborage and access for rodents and rodent active signs in the study area.

<p>(A and B) Photographs of the typical environment at the community study site, which shows a valley in which households are situated and the proximity of households to open sewers, exposed garbage and bushes or shrubbery. (C and D) Rodent burrows. (D and E) Rodent runs. (F) <i>Rattus norvegicus</i> fecal droppings.</p

Spatiotemporal determinants of urban Leptospirosis transmission:four-year prospective cohort study of slum residents in Brazil

Background Rat-borne leptospirosis is an emerging zoonotic disease in urban slum settlements for which there are no adequate control measures. The challenge in elucidating risk factors and informing approaches for prevention is the complex and heterogeneous environment within slums, which vary at fine spatial scales and influence transmission of the bacterial agent. Methodology/Principal Findings We performed a prospective study of 2,003 slum residents in the city of Salvador, Brazil during a four-year period (2003–2007) and used a spatiotemporal modelling approach to delineate the dynamics of leptospiral transmission. Household interviews and Geographical Information System surveys were performed annually to evaluate risk exposures and environmental transmission sources. We completed annual serosurveys to ascertain leptospiral infection based on serological evidence. Among the 1,730 (86%) individuals who completed at least one year of follow-up, the infection rate was 35.4 (95% CI, 30.7–40.6) per 1,000 annual follow-up events. Male gender, illiteracy, and age were independently associated with infection risk. Environmental risk factors included rat infestation (OR 1.46, 95% CI, 1.00–2.16), contact with mud (OR 1.57, 95% CI 1.17–2.17) and lower household elevation (OR 0.92 per 10m increase in elevation, 95% CI 0.82–1.04). The spatial distribution of infection risk was highly heterogeneous and varied across small scales. Fixed effects in the spatiotemporal model accounted for the majority of the spatial variation in risk, but there was a significant residual component that was best explained by the spatial random effect. Although infection risk varied between years, the spatial distribution of risk associated with fixed and random effects did not vary temporally. Specific “hot-spots” consistently had higher transmission risk during study years. Conclusions/Significance The risk for leptospiral infection in urban slums is determined in large part by structural features, both social and environmental. Our findings indicate that topographic factors such as household elevation and inadequate drainage increase risk by promoting contact with mud and suggest that the soil-water interface serves as the environmental reservoir for spillover transmission. The use of a spatiotemporal approach allowed the identification of geographic outliers with unexplained risk patterns. This approach, in addition to guiding targeted community-based interventions and identifying new hypotheses, may have general applicability towards addressing environmentally-transmitted diseases that have emerged in complex urban slum settings. Author Summary Leptospirosis is a rat-borne infectious disease that occurs worldwide, predominantly among vulnerable populations, such as urban slum communities with poor sanitation infrastructure. However, urban slums are complex local settings, where transmission of the disease varies over space and time, and the factors that influence this risk difference are unknown. An improved understanding of the environmental and social factors that modify the risk of this infection is needed in order to guide interventions to reduce the disease burden. We recruited a cohort of 2003 community residents of a high- risk urban slum in Salvador, Brazil. We followed them for a four-year period to understand yearly variation in individual and spatial risk factors for infection using spatiotemporal statistical modeling techniques. Our findings suggest that environmental factors related to topology such as household elevation and inadequate sewage drainage systems increase the risk of transmission in the slum microenvironment by promoting contact with mud contaminated with the pathogenic leptospiral bacteria, and that individual characteristics such as age and gender increase risk through behaviors that lead to increased exposures to a contaminated environment. Through this technique, we also identified local geographic areas where the risks are not well explained by these factors. This will help generate new hypotheses and identify intervention strategies for targeted prevention of leptospirosis in urban slum populations

Prospective Study of Leptospirosis Transmission in an Urban Slum Community: Role of Poor Environment in Repeated Exposures to the <i>Leptospira</i> Agent

<div><p>Background</p><p>Leptospirosis has emerged as an urban health problem as slum settlements have rapidly spread worldwide and created conditions for rat-borne transmission. Prospective studies have not been performed to determine the disease burden, identify risk factors for infection and provide information needed to guide interventions in these marginalized communities.</p><p>Methodology/Principal Findings</p><p>We enrolled and followed a cohort of 2,003 residents from a slum community in the city of Salvador, Brazil. Baseline and one-year serosurveys were performed to identify primary and secondary <i>Leptospira</i> infections, defined as respectively, seroconversion and four-fold rise in microscopic agglutination titers. We used multinomial logistic regression models to evaluate risk exposures for acquiring primary and secondary infection. A total of 51 <i>Leptospira</i> infections were identified among 1,585 (79%) participants who completed the one-year follow-up protocol. The crude infection rate was 37.8 per 1,000 person-years. The secondary infection rate was 2.3 times higher than that of primary infection rate (71.7 and 31.1 infections per 1,000 person-years, respectively). Male gender (OR 2.88; 95% CI 1.40–5.91) and lower per capita household income (OR 0.54; 95% CI, 0.30–0.98 for an increase of $1 per person per day) were independent risk factors for primary infection. In contrast, the 15–34 year age group (OR 10.82, 95% CI 1.38–85.08), and proximity of residence to an open sewer (OR 0.95; 0.91–0.99 for an increase of 1 m distance) were significant risk factors for secondary infection.</p><p>Conclusions/Significance</p><p>This study found that slum residents had high risk (>3% per year) for acquiring a <i>Leptospira</i> infection. Re-infection is a frequent event and occurs in regions of slum settlements that are in proximity to open sewers. Effective prevention of leptospirosis will therefore require interventions that address the infrastructure deficiencies that contribute to repeated exposures among slum inhabitants.</p></div

Age-specific attack rates for A) overall <i>Leptospira</i> infection according to gender [light grey bars, male; dark grey bars, female], and B) primary and secondary <i>Leptospira</i> infection rates [open bars, primary infection; black bars, secondary infection].

<p>Whiskers indicate the 95% Confidence Interval for the rate, adjusted for the survey design. The x axes refer to age groups in years. Rates in y axes are shown as infections per 1,000 person-years</p