The changing triad of plague in Uganda: invasive black rats(Rattus rattus), indigenous small mammals, and their fleas

Abstract

Rattus rattus was first reported from the West Nile Region of Uganda in 1961, an event that preceded the appearance of the first documented human plague outbreak in 1970. We investigated how invasive R. rattus and native small mammal populations, as well as their fleas, have changed in recent decades. Over an 18‐month period, a total of 2,959 small mammals were captured, sampled, and examined for fleas, resulting in the identification of 20 small mammal taxa that were hosts to 5,109 fleas (nine species). Over three‐fourths (75.8%) of captured mammals belonged to four taxa: R. rattus, which predominated inside huts, and Arvicanthis niloticus, Mastomys sp., and Crocidura sp., which were more common outside huts. These mammals were hosts for 85.8% of fleas collected, including the efficient plague vectors Xenopsylla cheopis and X. brasiliensis, as well as likely enzootic vectors, Dinopsyllus lypusus and Ctenophthalmus bacopus. Flea loads on small mammals were higher in certain environments in villages with a recent history of plague compared to those that lacked such a history. The significance of these results is discussed in relation to historical data, the initial spread of plague in the WNR and the continuing threat posed by the disease.

A Novel Loop-Mediated Isothermal Amplification Assay for Rapid Detection of Yersinia pestis

“…Serology is mainly used in late stages of the infection for detection of plague antibodies ( Splettstoesser et al, 2004 ; Simon et al, 2013 ; Hsu et al, 2018 ). While useful for identifying evidence of past plague activity, serology is not suitable for investigating plague in rodents due to the extremely high mortality ( Enscore et al, 2020 ). In recent years, polymerase chain reaction (PCR) and other molecular diagnostic techniques have been developed and largely applied for Y. pestis detection ( Campbell et al, 1993 ; Neubauer et al, 2000 ; Tomaso et al, 2003 ; Stewart et al, 2008 ; Bai et al, 2020 ).…”

Epidemiology, Ecology and Prevention of Plague in the West Nile Region of Uganda: The Value of Long-Term Field Studies

“…12 Although we cannot rule out the possibility that Y. pestis was circulating in sylvatic cycles before recognition of human cases, the introduction of R. rattus and its establishment as the primary hut-dwelling species, replacing Mastomys sp., might explain changes in human risk of exposure to Y. pestis. 29 Recent field surveys revealed that R. rattus is the predominant small mammal captured within huts. 16,25,[27][28][29][30][31][32][33][34] R. rattus is known to be susceptible to Y. pestis and is often viewed as an important amplifying host.…”

“…29 Recent field surveys revealed that R. rattus is the predominant small mammal captured within huts. 16,25,[27][28][29][30][31][32][33][34] R. rattus is known to be susceptible to Y. pestis and is often viewed as an important amplifying host. 3 Indeed, Y. pestis has been isolated from numerous R. rattus carcasses from the WNR, 35 but serological evidence to suggest they survive plague infection in this region is lacking.…”

“…39 In the WNR, host and flea diversity increase with distance away from huts, supporting the prevailing hypothesis that in east Africa, Y. pestis is maintained in enzootic cycles in the bush and that the bacteria occasionally spill over to rats in the hut environment. [27][28][29] Seroprevalence is typically low (< 1%) in small mammals. However, positive results from Arvicanthis niloticus and Crocidura spp.…”

“…28 In addition, the heavy flea infestation and diversity of fleas infesting A. niloticus, as well as the observation that their abundance increases seasonally inside the plague focus, but not outside, provides support for the assumption that it is a key host in Y. pestis transmission outside of homes. 20,[27][28][29] Environmental surveillance and plague prevention. Plague occurs sporadically and at low incidence, and resources for surveillance and prevention often compete with other diseases of greater incidence, stressing the need for environmental surveillance and control approaches to be low cost or provide additional collateral public health benefits.…”