Socio-ecological risk factors associated with human flea infestations of rural household in plague-endemic areas of Madagascar

Plague is a flea-borne fatal disease caused by the bacterium Yersinia pestis, which persists in rural Madagascar. Although fleas parasitizing rats are considered the primary vectors of Y. pestis, the human flea, Pulex irritans, is abundant in human habitations in Madagascar, and has been found naturally infected by the plague bacterium during outbreaks. While P. irritans may therefore play a role in plague transmission if present in plague endemic areas, the factors associated with infestation and human exposure within such regions are little explored. To determine the socio-ecological risk factors associated with P. irritans infestation in rural households in plague-endemic areas of Madagascar, we used a mixed-methods approach, integrating results from P. irritans sampling, a household survey instrument, and an observational checklist. Using previously published vectorial capacity data, the minimal P. irritans index required for interhuman bubonic plague transmission was modeled to determine whether household infestations were enough to pose a plague transmission risk. Socio-ecological risk factors associated with a high P. irritans index were then identified for enrolled households using generalized linear models. Household flea abundance was also modeled using the same set of predictors. A high P. irritans index occurred in approximately one third of households and was primarily associated with having a traditional dirt floor covered with a plant fiber mat. Interventions targeting home improvement and livestock housing management may alleviate flea abundance and plague risk in rural villages experiencing high P. irritans infestation. As plague-control resources are limited in developing countries such as Madagascar, identifying the household parameters and human behaviors favoring flea abundance, such as those identified in this study, are key to developing preventive measures that can be implemented at the community level. Plague is a bacterial disease transmitted by flea bites, and the rat fleas are the main vectors of Yersinia pestis, the plague bacterium. Households in plague endemic-areas of Madagascar are frequently infested by Pulex irritans, the human flea, which does become naturally infected with the plague bacterium during epidemic. The intensity of flea infestation varies among households, but the reasons for such disparities are poorly understood. This study identifies factors associated with P. irritans infestation in rural households in plague-endemic areas of Madagascar. Infestation risk was more pronounced for poor households living in homes made with organic construction materials and flea density did not show a seasonal pattern. One third of the household experienced high flea infestation, putting inhabitants at risk of sustained interhuman plague transmission, should the fleas or a household member become infected. While P. irritans may be a secondary vector, this additional route of plague transmission deserves more attention from epidemiologists. The factors identified in this analysis suggest that improvement of housing and better management of livestock would alleviate flea burden and potential plague risk in rural plague-endemic villages experiencing high flea infestation.