Comparison of Zoonotic Bacterial Agents in Fleas Collected from Small Mammals or Host-Seeking Fleas from a Ugandan Region Where Plague Is Endemic.

Ying Bai,Lynn M Osikowicz,Karen A Boegler,Kenneth L Gage,Michael Y Kosoy,Rebecca J Eisen,Linda A Atiku,Russell E Enscore,Joseph T Mpanga,Karen L Visick

doi:10.1128/msphere.00402-17

Ying Bai, Lynn M Osikowicz + Show 8 more

Open Access

https://doi.org/10.1128/msphere.00402-17

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Abstract

Fleas (n = 407) were collected from small mammals trapped inside huts and surroundings of homesteads in five villages within the Arua and Zombo districts of Uganda. The most common flea species were Dinopsyllus lypusus (26%) and Xenopsylla cheopis (50%). Off-host fleas (n = 225) were collected inside huts by using Kilonzo flea traps. The majority of the off-host fleas were Ctenocephalides felis (80%). All fleas were examined for the presence of Bartonella spp., Rickettsia spp., and Yersinia spp. Bartonella DNA was detected in 91 fleas, with an overall prevalence of 14%. Bartonella prevalence was significantly higher in rodent or shrew fleas than in off-host fleas (22% versus 1%). The majority of Bartonella-positive fleas were of the species D.lypusus (61%), X.cheopis (20%), and Ctenophthalmus calceatus (14%). Sequencing analysis identified 12 Bartonella genetic variants, 9 of which belonged to the zoonotic pathogen B.elizabethae species complex. Rickettsia DNA was detected in 143 fleas, giving an overall prevalence of 23%, with a significantly higher prevalence in off-host fleas than in rodent or shrew fleas (56% versus 4%). The majority (88%) of Rickettsia-positive fleas were C.felis and were collected from Kilonzo traps, while a small portion (10%) were X.cheopis collected from rodents. Sequencing analysis identified six Rickettsia genogroups that belonged either to zoonotic R.felis or to the closely related "Candidatus Ricksettiaasemboensis" and "Candidatus Ricksettiasengalensis." Yersinia DNA was not detected in the fleas tested. These observations suggested that fleas in northwestern Uganda commonly carry the zoonotic agents B.elizabethae and R.felis and potentially play an important role in transmitting these infections to humans. IMPORTANCE Fleas play critical roles in transmitting some infections among animals and from animals to humans. Detection of pathogens in fleas is important to determine human risks for flea-borne diseases and can help guide diagnosis and treatment. Our findings of high prevalence rates of B.elizabethae and R.felis in fleas in the Arua and Zombo districts of Uganda implicate these agents as potential causative agents of undiagnosed febrile illnesses in this area.

Highlights

IMPORTANCE Fleas play critical roles in transmitting some infections among animals and from animals to humans
The fleas belonged to eight species, including Ctenocephalides felis (n ϭ 1), Ctenophthalmus calceatus (n ϭ 44), Dinopsyllus longifrons (n ϭ 2), D. lypusus (n ϭ 106), Stivalius torvus (n ϭ 11), Xenopsylla brasiliensis (n ϭ 40), X. cheopis (n ϭ 202), and Xenopsylla nubica (n ϭ 1) (Table 1)
Using molecular approaches, we estimated the presence of multiple potential zoonotic pathogens, including Bartonella spp., Rickettsia spp., and Yersinia spp., in fleas collected from small mammals and those that were host seeking in human habitations in northwestern Uganda, where plague is endemic and occasionally causes outbreaks in the local human population [28]

Summary

Introduction

IMPORTANCE Fleas play critical roles in transmitting some infections among animals and from animals to humans. Rickettsia felis, the causative agent of flea-borne spotted fever, is considered an important neglected agent in sub-Saharan Africa [12]. Both bartonelloses and rickettsioses are widely regarded as emerging/reemerging diseases [13]. Many studies have reported Bartonella spp. in a variety of mammalian species and their ectoparasites, all over the world [14,15,16,17,18,19,20]. The prevalence of Bartonella infections in invasive rats (Rattus rattus) reported in that study was very low (1.3%), a finding that stands in stark contrast to results of a study conducted in neighboring Kenya, in which the Bartonella prevalence was 13% in Rattus spp. R. felis and “Candidatus Rickettsia asemboensis” were detected in fleas collected in Kenya, Tanzania, Ethiopia, and Uganda [13, 23,24,25]

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