Elucidating transmission dynamics and host-parasite-vector relationships for rodent-borne Bartonella spp. in Madagascar

Cara E Brook,Ying Bai,Emily O Yu,Hafaliana C Ranaivoson,Haewon Shin,Andrew P Dobson,C Jessica E Metcalf,Michael Y Kosoy,Katharina Dittmar

doi:10.1016/j.epidem.2017.03.004

Abstract

Bartonella spp. are erythrocytic bacteria transmitted via arthropod vectors, which infect a broad range of vertebrate hosts, including humans. We investigated transmission dynamics and host-parasite-vector relationships for potentially zoonotic Bartonella spp. in invasive Rattus rattus hosts and associated arthropod ectoparasites in Madagascar. We identified five distinct species of Bartonella (B. elizabethae 1, B. elizabethae 2, B. phoceensis 1, B. rattimassiliensis 1, and B. tribocorum 1) infecting R. rattus rodents and their ectoparasites. We fit standard epidemiological models to species-specific age-prevalence data for the four Bartonella spp. with sufficient data, thus quantifying age-structured force of infection. Known zoonotic agents, B. elizabethae 1 and 2, were best described by models exhibiting high forces of infection in early age class individuals and allowing for recovery from infection, while B. phoceensis 1 and B. rattimassiliensis 1 were best fit by models of lifelong infection without recovery and substantially lower forces of infection. Nested sequences of B. elizabethae 1 and 2 were recovered from rodent hosts and their Synopsyllus fonquerniei and Xenopsylla cheopsis fleas, with a particularly high prevalence in the outdoor-dwelling, highland-endemic S. fonquerniei. These findings expand on force of infection analyses to elucidate the ecological niche of the zoonotic Bartonella elizabethae complex in Madagascar, hinting at a potential vector role for S. fonquerniei. Our analyses underscore the uniqueness of such ecologies for Bartonella species, which pose a variable range of potential zoonotic threats.

Highlights

Bartonella spp. are facultative, intracellular Gram-negative bacteria, which infect the endothelial cells and erythrocytes of a broad diversity of vertebrate hosts
A three-age class SIS model offered the best fit for B. elizabethae 1 and 2 genotypes, while an SI model with constant force of infection (FOI) best represented the B. phoceensis 1 data
Like B. phoceensis 1, the B. rattimassiliensis 1 data were best described by an SI model, though inclusion of age structure here significantly improved the model’s ability to recover patterns in the data

Summary

Introduction

Bartonella spp. are facultative, intracellular Gram-negative bacteria, which infect the endothelial cells and erythrocytes of a broad diversity of vertebrate hosts. At least twelve known species or subspecies of Bartonella bacteria are recognized zoonotic agents (VayssierTaussat et al, 2009; Veikkolainen et al, 2014), and two others, B. bacilliformis and B. quintana (respectively, the causative agents for Carrion’s disease and trench fever) can maintain transmission in human hosts (Vayssier-Taussat et al, 2009). Zoonotic Bartonella spp. typically cause fever, lymphadenopathy, skin lesions, cardiopathy, endocarditis, or neuroretinitis in humans (Breitschwerdt and Kordick, 2000; Kosoy et al, 2003), as exemplified by Bartonella henselae, the causative agent in Cat Scratch Disease (Welch et al, 1992). Among Bartonella spp., B. bacilliformis (previously identified only in humans and sandfly vectors) is an exception in causing widespread and life-threatening hemolytic anemia in its primary host (Ihler, 1996)

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