Spatiotemporal Determinants of Urban Leptospirosis Transmission

Four-Year Prospective Cohort Study of Slum Residents in Brazil

José E. Hagan, Paula Moraga, Federico Costa, Nicolas Capian, Guilherme S. Ribeiro, Elsio A. Wunder, Ridalva D M Felzemburgh, Renato B. Reis, Nivison Nery, Francisco S. Santana, Deborah Fraga, Balbino L. dos Santos, Andréia C. Santos, Adriano Queiroz, Wagner Tassinari, Marilia S. Carvalho, Mitermayer G. Reis, Peter J. Diggle, Albert I. Ko

Research output: Contribution to journalArticle

Abstract

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.

Original languageEnglish (US)
Article numbere0004275
JournalPLoS Neglected Tropical Diseases
Volume10
Issue number1
DOIs
StatePublished - Jan 15 2016
Externally publishedYes

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Poverty Areas
Leptospirosis
Brazil
Cohort Studies
Prospective Studies
Infection
Geographic Information Systems
Environmental Exposure
Zoonoses
Drainage
Soil
Interviews

ASJC Scopus subject areas

  • Infectious Diseases
  • Public Health, Environmental and Occupational Health
  • Pharmacology, Toxicology and Pharmaceutics(all)

Cite this

Spatiotemporal Determinants of Urban Leptospirosis Transmission : Four-Year Prospective Cohort Study of Slum Residents in Brazil. / Hagan, José E.; Moraga, Paula; Costa, Federico; Capian, Nicolas; Ribeiro, Guilherme S.; Wunder, Elsio A.; Felzemburgh, Ridalva D M; Reis, Renato B.; Nery, Nivison; Santana, Francisco S.; Fraga, Deborah; dos Santos, Balbino L.; Santos, Andréia C.; Queiroz, Adriano; Tassinari, Wagner; Carvalho, Marilia S.; Reis, Mitermayer G.; Diggle, Peter J.; Ko, Albert I.

In: PLoS Neglected Tropical Diseases, Vol. 10, No. 1, e0004275, 15.01.2016.

Research output: Contribution to journalArticle

Hagan, JE, Moraga, P, Costa, F, Capian, N, Ribeiro, GS, Wunder, EA, Felzemburgh, RDM, Reis, RB, Nery, N, Santana, FS, Fraga, D, dos Santos, BL, Santos, AC, Queiroz, A, Tassinari, W, Carvalho, MS, Reis, MG, Diggle, PJ & Ko, AI 2016, 'Spatiotemporal Determinants of Urban Leptospirosis Transmission: Four-Year Prospective Cohort Study of Slum Residents in Brazil', PLoS Neglected Tropical Diseases, vol. 10, no. 1, e0004275. https://doi.org/10.1371/journal.pntd.0004275
Hagan, José E. ; Moraga, Paula ; Costa, Federico ; Capian, Nicolas ; Ribeiro, Guilherme S. ; Wunder, Elsio A. ; Felzemburgh, Ridalva D M ; Reis, Renato B. ; Nery, Nivison ; Santana, Francisco S. ; Fraga, Deborah ; dos Santos, Balbino L. ; Santos, Andréia C. ; Queiroz, Adriano ; Tassinari, Wagner ; Carvalho, Marilia S. ; Reis, Mitermayer G. ; Diggle, Peter J. ; Ko, Albert I. / Spatiotemporal Determinants of Urban Leptospirosis Transmission : Four-Year Prospective Cohort Study of Slum Residents in Brazil. In: PLoS Neglected Tropical Diseases. 2016 ; Vol. 10, No. 1.
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abstract = "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.",
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T1 - Spatiotemporal Determinants of Urban Leptospirosis Transmission

T2 - Four-Year Prospective Cohort Study of Slum Residents in Brazil

AU - Hagan, José E.

AU - Moraga, Paula

AU - Costa, Federico

AU - Capian, Nicolas

AU - Ribeiro, Guilherme S.

AU - Wunder, Elsio A.

AU - Felzemburgh, Ridalva D M

AU - Reis, Renato B.

AU - Nery, Nivison

AU - Santana, Francisco S.

AU - Fraga, Deborah

AU - dos Santos, Balbino L.

AU - Santos, Andréia C.

AU - Queiroz, Adriano

AU - Tassinari, Wagner

AU - Carvalho, Marilia S.

AU - Reis, Mitermayer G.

AU - Diggle, Peter J.

AU - Ko, Albert I.

PY - 2016/1/15

Y1 - 2016/1/15

N2 - 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.

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