Browsing by Author "Gage, Kenneth L."
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Item Bartonella Species in Invasive Rats and Indigenous Rodents from Uganda(Vector-Borne and Zoonotic Diseases, 2014) Borchert, Jeff N.; Atiku, Linda A.; Mpanga, Joseph T.; Gage, Kenneth L.; Kosoy, Michael Y.; Billeter, Sarah A.The presence of bartonellae in invasive rats (Rattus rattus) and indigenous rodents (Arvicanthis niloticus and Cricetomys gambianus) from two districts in Uganda, Arua and Zombo, was examined by PCR detection and culture. Blood from a total of 228 R. rattus, 31 A. niloticus, and 5 C. gambianus was screened using genus- specific primers targeting the 16S–23S intergenic spacer region. Furthermore, rodent blood was plated on brain heart infusion blood agar, and isolates were verified as Bartonella species using citrate synthase gene- (gltA) specific primers. One hundred and four fleas recovered from R. rattus were also tested for the presence of Bartonella species using the same gltA primer set. An overall prevalence of 1.3% (three of 228) was obtained in R. rattus, whereas 61.3% of 31 A. niloticus and 60% of five C. gambianus were positive for the presence The presence of bartonellae in invasive rats (Rattus rattus) and indigenous rodents (Arvicanthis niloticus and Cricetomys gambianus) from two districts in Uganda, Arua and Zombo, was examined by PCR detection and culture. Blood from a total of 228 R. rattus, 31 A. niloticus, and 5 C. gambianus was screened using genus-specific primers targeting the 16S–23S intergenic spacer region. Furthermore, rodent blood was plated on brain heart infusion blood agar, and isolates were verified as Bartonella species using citrate synthase gene- (gltA) specific primers. One hundred and four fleas recovered from R. rattus were also tested for the presence of Bartonella species using the same gltA primer set. An overall prevalence of 1.3% (three of 228) was obtained in R. rattus, whereas 61.3% of 31 A. niloticus and 60% of five C. gambianus were positive for the presence of Bartonella species. Genotypes related to Bartonella elizabethae, a known zoonotic pathogen, were detected in three R. rattus and one C. gambianus. Bartonella strains, similar to bacteria detected in indigenous rodents from other African countries, were isolated from the blood of A. niloticus. Bartonellae, similar to bacteria initially cultured from Ornithodorus sonrai (soft tick) from Senegal, were found in two C. gambianus. Interestingly, bartonellae detected in fleas from invasive rats were similar to bacteria identified in indigenous rodents and not their rat hosts, with an overall prevalence of 6.7%. These results suggest that if fleas are competent vectors of these bartonellae, humans residing in these two districts of Uganda are potentially at greater risk for exposure to Bartonella species from native rodents than from invasive rats. The low prevalence of bartonellae in R. rattus was quite surprising, in contrast, to the detection of these organisms in a large percentage of Rattus species from other geographical areas. A possible reason for this disparity is discussed of Bartonella species. Genotypes related to Bartonella elizabethae, a known zoonotic pathogen, were detected in three R. rattus and one C. gambianus. Bartonella strains, similar to bacteria detected in indigenous rodents from other African countries, were isolated from the blood of A. niloticus. Bartonellae, similar to bacteria initially cultured from Ornithodorus sonrai (soft tick) from Senegal, were found in two C. gambianus. Interestingly, bartonellae detected in fleas from invasive rats were similar to bacteria identified in indigenous rodents and not their rat hosts, with an overall prevalence of 6.7%. These results suggest that if fleas are competent vectors of these bartonellae, humans residing in these two districts of Uganda are potentially at greater risk for exposure to Bartonella species from native rodents than from invasive rats. The low prevalence of bartonellae in R. rattus was quite surprising, in contrast, to the detection of these organisms in a large percentage of Rattus species from other geographical areas. A possible reason for this disparity is discussedItem Blood Meal Identification in Off-Host Cat Fleas (Ctenocephalides felis) from a Plague-Endemic Region of Uganda(The American journal of tropical medicine and hygiene, 2013) Graham, Christine B.; Borchert, Jeff N.; Black IV, William C.; Atiku, Linda A.; Mpanga, Joseph T.; Boegler, Karen A.; Moore, Sean M.; Gage, Kenneth L.; Eisen, Rebecca J.The cat flea, Ctenocephalides felis, is an inefficient vector of the plague bacterium (Yersinia pestis) and is the predominant off-host flea species in human habitations in the West Nile region, an established plague focus in Northwest Uganda. To determine if C. felis might serve as a Y. pestis bridging vector in the West Nile region, we collected on- and off-host fleas from human habitations and used a real-time polymerase chain reaction-based assay to estimate the proportion of off-host C. felis that had fed on humans and the proportion that had fed on potentially infectious rodents or shrews. Our findings indicate that cat fleas in human habitations in the West Nile region feed primarily on domesticated species. We conclude that C. felis is unlikely to serve as a Y. pestis bridging vector in this region.Item Early-phase Transmission of Yersinia pestis by Cat Fleas (Ctenocephalides felis) and Their Potential Role as Vectors in a Plague-endemic Region of Uganda(The American journal of tropical medicine and hygiene, 2008) Eisen, Rebecca J.; Borchert, Jeff N.; Holmes, Jennifer L.; Amatre, Gerald; Van Wyk, Kristen; Enscore, Russell E.; Babi, Nackson; Atiku, Linda A.; Wilder, Aryn P.; Vetter, Sara M.; Bearden, Scott W.; Montenieri, John A.; Gage, Kenneth L.In recent decades, the majority of human plague cases (caused by Yersinia pestis) have been reported from Africa. In northwest Uganda, which has had recent plague outbreaks, cat fleas (Ctenocephalides felis) have been reported as the most common fleas in the home environment, which is suspected to be a major exposure site for human plague in this country. In the past, C. felis has been viewed as only a nuisance-biting insect because limited laboratory studies suggested it is incapable of transmitting Y. pestis or is an inefficient vector. Our laboratory study shows that C. felis is a competent vector of plague bacteria, but that efficiency is low compared with another flea species collected in the same area: the oriental rat flea, Xenopsylla cheopis. On the other hand, despite its low vector efficiency, C. felis is the most common flea in human habitations in a plague-endemic region of Uganda (Arua and Nebbi Districts), and occasionally infests potential rodent reservoirs of Y. pestis such as the roof rat (Rattus rattus) or the Nile rat (Arvicanthisniloticus). Plague control programs in this region should remain focused on reducing rat flea populations, although our findings imply that cat fleas should not be ignored by these programs as they could play a significant role as secondary vectors.Item Efficacy of Indoor Residual Spraying Using Lambda-Cyhalothrin for Controlling Nontarget Vector Fleas (Siphonaptera) on Commensal Rats in a Plague Endemic Region of Northwestern Uganda(Journal of medical entomology, 2014) Borchert, Jeff N.; Eisen, Rebecca J.; Atiku, Linda A.; Delorey, Mark J.; Mpanga, Joseph T.; Babi, Nackson; Gage, Kenneth L.; Enscore, Russell E.Over the past two decades, the majority ofhumanplague cases have been reported from areas in Africa, including Uganda. In an effort to develop affordable plague control methods within an integrated vector control framework, we evaluated the efÞcacy of indoor residual spraying (IRS) techniques commonly used for mosquito control for controlling ßeas on hut-dwelling commensal rodents in a plague-endemic region of Uganda. We evaluated both the standard IRS spraying (walls and ceiling) and a modiÞed IRS technique that included insecticide application on not only on walls and ceiling but also a portion of the ßoor of each treated hut. Our study demonstrated that both the standard and modiÞed IRS applications were effective at signiÞcantly reducing the ßea burden and ßea infestation of commensal rodents for up to 100 d after application, suggesting that IRS could potentially provide simultaneous control of mosquito and ßeaborne diseases.Item Epidemiology, Ecology and Prevention of Plague in the West Nile Region of Uganda: The Value of Long-Term Field Studies(The American Journal of Tropical Medicine and Hygiene., 2021) Eisen, Rebecca J.; Atiku, Linda A.; Enscore, Russell E.; Mpanga, Joseph T.; Acayo, Sarah; Mead, Paul S.; Apangu, Titus; Yockey, Brook M.; Borchert, Jeff N.; Beard, Charles B.; Gage, Kenneth L.Plague, a fleaborne rodent-associated zoonosis, is a neglected disease with most recent cases reported from east and central Africa and Madagascar. Because of its low incidence and sporadic occurrence, most of our knowledge of plague ecology, prevention, and control derives from investigations conducted in response to human cases. Long-term studies (which are uncommon) are required to generate data to support plague surveillance, prevention, and control recommendations. Here we describe a 15-year, multidisciplinary commitment to plague in the West Nile region of Uganda that led to significant advances in our understanding of where and when persons are at risk for plague infection and how to reduce morbidity and mortality. These findings provide data-driven support for several existing recommendations on plague surveillance and prevention and may be generalizable to other plague fociItem Evaluation and Modification of Off-Host Flea Collection Techniques Used in Northwest Uganda: Laboratory and Field Studies(Journal of medical entomology, 2012) Borchert, Jeff N.; Eisen, Rebecca J.; Holmes, Jennifer L.; Atiku, Linda A.; Mpanga, Joseph T.; Brown, Heidi E.; Graham, Christine B.; Babi, Nackson; Montenieri, John A.; Enscore, Russell E.; Gage, Kenneth L.Quantifying the abundance of host-seeking ßeas is critical for assessing risk of human exposure to ßea-borne disease agents, including Yersinia pestis, the etiological agent of plague. Yet, reliable measures of the efÞcacy of existing host-seeking ßea collection methods are lacking. In this study, we compare the efÞcacy of passive and active methods for the collection of host-seeking ßeas in both the laboratory and human habitations in a plague-endemic region of northwest Uganda. In the laboratory, lighted “Kilonzo” ßea traps modiÞed with either blinking lights, the creation of shadows or the generation of carbon dioxide were less efÞcient at collecting Xenopsylla cheopis Rothchild and Ctenocephalides felis Bouche´ ßeas than an active collection method using white cotton socks or cotton ßannel. Passive collection using Kilonzo light traps in the laboratory collected signiÞcantly more X. cheopis than C. felis and active collection, using white socks and ßannel, collected signiÞcantly more C. felis than X. cheopis. In Þeld studies conducted in Uganda, Kilonzo traps using a ßashlight were similar in their collection efÞcacy to Kilonzo traps using kerosene lamps. However, in contrast to laboratory studies, Kilonzo ßea traps using ßashlights collected a greater number of ßeas than swabbing. Within human habitations in Uganda, Kilonzo traps were especially useful for collecting C. felis, the dominant species found in human habitations in this area.Item An Evaluation of Removal Trapping to Control Rodents Inside Homes in a Plague-Endemic Region of Rural Northwestern Uganda(Vector-Borne and Zoonotic Diseases, 2018) Eisen, Rebecca J.; Atiku, Linda A.; Boegler, Karen A.; Mpanga, Joseph T.; Enscore, Russell E.; MacMillan, Katherine; Gage, Kenneth L.Rodents pose a significant threat to human health, particularly in rural subsistence farming communities in Africa, where rodents threaten food security and serve as reservoirs of human pathogens, including the agents of plague, leptospirosis, murine typhus, rat-bite fever, Lassa fever, salmonellosis, and campylobacteriosis. Our study focused on the plague-endemic West Nile region of Uganda, where a majority of residents live in Uganda government-defined poverty, rely on subsistence farming for a living, and frequently experience incursions of rodents into their homes. In this study, we show that rodent removal was achieved in a median of 6 days of intensive lethal trapping with multiple trap types (range: 0–16 days). However, rodent abundance in 68.9% of homesteads returned to pretreatment levels within a median of 8 weeks (range 1–24 weeks), and at least a single rodent was captured in all homesteads by a median of 2 weeks (range 1–16 weeks) after removal efforts were terminated. Results were similar between homesteads that practiced rodent control whether or not their neighbors implemented similar strategies. Overall, intensive lethal trapping inside homes appears to be effective at reducing rodent abundance, but control was short lived after trapping ceased.Item Evaluation of Rodent Bait Containing Imidacloprid for the Control of Fleas on Commensal Rodents in a Plague-Endemic Region of Norther Uganda(Journal of medical entomology, 2010) Borchert, Jeff; Enscore, Russell E.; Eisen Rebecca J.; Atiku, Linda A.; Owor, Nicholas; Acayo, Sarah; Babi, Nackson; Montenieri, John A.; Gage, Kenneth L.In recent decades, the majority of human plague cases (caused by Yersinia pestis) have been reported from Africa. In an effort to reduce the risk of the disease in this area, we evaluated theefÞcacy of a host-targeted rodent bait containing the insecticide imidacloprid for controlling ßeas on house-dwelling commensal rodents in a plague-endemic region of northwestern Uganda. results demonstrated that the use of a palatable, rodent-targeted, wax-based bait cube was effective at reducing the prevalence of ßeas on commensal rodents and ßea burdens on these animals at day 7 postbait exposure, but lacked signiÞcant residual activity, allowing ßea populations to rebound in the absence of additional bait applications. Our results indicate the use of a palatable host-targeted bait block containing imidacloprid was an effective technique for quickly reducing ßea numbers on rodents in northwest Uganda and, thus, could be useful for lowering the potential risk of human ßea bite exposures during plague outbreaks if applied continuously during the period of riskItem Flea Diversity and Infestation Prevalence on Rodents in a Plague-Endemic Region of Uganda(The American journal of tropical medicine and hygiene, 2009) Amatre, Gerald; Babi, Nackson; Enscore, Russell E.; Ogen-Odoi, Asaph; Atiku, Linda A.; Akol, Anne; Gage, Kenneth L.; Eisen, Rebecca J.In Uganda, the West Nile region is the primary epidemiologic focus for plague. The aims of this study wereto 1) describe flea–host associations within a plague-endemic region of Uganda, 2) compare flea loads between villages with or without a history of reported human plague cases and between sampling periods, and 3) determine vector loads on small mammal hosts in domestic, peridomestic, and sylvatic settings. We report that the roof rat, Rattusrattus, is the most common rodent collected in human dwellings in each of the 10 villages within the two districts sampled. These rats were commonly infested with efficient Y. pestis vectors, Xenopsylla cheopis and X. brasiliensis in Arua and Nebbi districts, respectively. In peridomestic and sylvatic areas in both districts, the Nile rat, Arvicanthus niloticus, was the most abundant rodent and hosted the highest diversity of flea species. When significant temporal differences in flea loads were detected, they were typically lower during the dry month of January. We did not detect any significant differences in small mammal abundance or flea loads between villages with our without a history of human plague, indicating that conditions during inter-epizootic periods are similar between these areas. Future studies are needed to determine whether flea abundance or species composition changes during epizootics when humans are most at risk of exposure.Item Flea Diversity as an Element for Persistence of Plague Bacteria in an East African Plague Focus(PLoS ONE, 2012) Eisen, Rebecca J.; Borchert, Jeff N.; Mpanga, Joseph T.; Atiku, Linda A.; MacMillan, Katherine; Boegler, Karen A.; Montenieri, John A.; Monaghan, Andrew; Gage, Kenneth L.Plague is a flea-borne rodent-associated zoonotic disease that is caused by Yersinia pestis and characterized by long quiescent periods punctuated by rapidly spreading epidemics and epizootics. How plague bacteria persist during interepizootic periods is poorly understood, yet is important for predicting when and where epizootics are likely to occur and for designing interventions aimed at local elimination of the pathogen. Existing hypotheses of how Y. pestis is maintained within plague foci typically center on host abundance or diversity, but little attention has been paid to the importance of flea diversity in enzootic maintenance. Our study compares host and flea abundance and diversity along an elevation gradient that spans from low elevation sites outside of a plague focus in the West Nile region of Uganda (,725–1160 m) to higher elevation sites within the focus (,1380–1630 m). Based on a year of sampling, we showed that host abundance and diversity, as well as total flea abundance on hosts was similar between sites inside compared with outside the plague focus. By contrast, flea diversity was significantly higher inside the focus than outside. Our study highlights the importance of considering flea diversity in models of Y. pestis persistence.Item Identification of Flea Blood Meals Using Multiplexed Real-Time Polymerase Chain Reaction Targeting Mitochondrial Gene Fragments(The American journal of tropical medicine and hygiene, 2009) Woods, Michael E.; Montenieri, John A.; Eisen, Rebecca J.; Zeidner, Nordin S.; Borchert, Jeff N.; Laudisoit, Anne; Babi, Nackson; Atiku, Linda A.; Enscore, Russell E.; Gage, Kenneth L.is found in the West Nile region of Uganda and Democratic Republic of the Congo where flea vectors are often found inhabiting homes. We have developed a multiplexed, real-time polymerase chain reaction assay targeting mitochondrial genes that is capable of detecting blood meal sources in fleas collected off-host in East Africa. Laboratory tests showed that the assay is specific for the intended targets and has a detection limit below one picogram of DNA. Testing of wild-caught fleas from the Democratic Republic of Congo suggests that humans are at significant risk from flea-borne disease and implicates domestic animals including cats, chickens, and the black rat as potential sources of human exposure to fleas and flea-borne diseases. Future application of the assay will help us better define the ecology of plague in East Africa to implement effective control measures to combat the spread of disease.Item Identification of Risk Factors for Plague in the West Nile Region of Uganda(The American journal of tropical medicine and hygiene, 2014) Eisen, Rebecca J.; MacMillan, Katherine; Atiku, Linda A; Mpanga, Joseph T.; Zielinski-Gutierrez, Emily; Graham, Christine B.; Boegler, Karen A.; Enscore, Russell E.; Gage, Kenneth L.Plague is an often fatal, primarily flea-borne rodent-associated zoonosis caused by Yersinia pestis. We sought to identify risk factors for plague by comparing villages with and without a history of human plague cases within a model-defined plague focus in the West Nile Region of Uganda. Although rat (Rattus rattus) abundance was similar inside huts within case and control villages, contact rates between rats and humans (as measured by reported rat bites) and host-seeking flea loads were higher in case villages. In addition, compared with persons in control villages, persons in case villages more often reported sleeping on reed or straw mats, storing food in huts where persons sleep, owning dogs and allowing them into huts where persons sleep, storing garbage inside or near huts, and cooking in huts where persons sleep. Compared with persons in case villages, persons in control villages more commonly reported replacing thatch roofing, and growing coffee, tomatoes, onions, and melons in agricultural plots adjacent to their homesteads. Rodent and flea control practices, knowledge of plague, distance to clinics, and most care-seeking practices were similar between persons in case villages and persons in control villages. Our findings reinforce existing plague prevention recommendations and point to potentially advantageous local interventions.Item Rat Fall Surveillance Coupled with Vector Control and Community Education as a Plague Prevention Strategy in the West Nile Region, Uganda(The American Society of Tropical Medicine and Hygiene, 2018) Boegler, Karen A.; Atiku, Linda A.; Enscore, Russell E.; Apangu, Titus; Tendo Mpanga, Joseph,; Acayo, Sarah; Kaggwa, John; Mead, Paul S.; Yockey, Brook M.; Kugeler, Kiersten J.; Schriefer, Martin E.; Horiuchi, Kalanthe; Gage, Kenneth L.; Eisen, Rebecca J.Plague, primarily a disease of rodents, is most frequently transmitted by fleas and causes potentially fatal infections in humans. In Uganda, plague is endemic to the West Nile region. Primary prevention for plague includes control of rodent hosts or flea vectors, but targeting these efforts is difficult given the sporadic nature of plague epizootics in the region and limited resource availability. Here, we present a community-based strategy to detect and report rodent deaths (rat fall), an early sign of epizootics. Laboratory testing of rodent carcasses is used to trigger primary and secondary prevention measures: indoor residual spraying (IRS) and community-based plague education, respectively. During the first 3 years of the program, individuals from 142 villages reported 580 small mammal deaths; 24 of these tested presumptive positive for Yersinia pestis by fluorescence microscopy. In response, for each of the 17 affected communities, village-wide IRS was conducted to control rodent-associated fleas within homes, and community sensitization was conducted to raise awareness of plague signs and prevention strategies. No additional presumptive Y. pestis-positive carcasses were detected in these villages within the 2-month expected duration of residual activity for the insecticide used in IRS. Despite comparatively high historic case counts, no human plague cases were reported from villages participating in the surveillance program; five cases were reported from elsewhere in the districts. Weevaluate community participation and timeliness of response, report the frequency of human plague cases in participating and surrounding villages, and evaluate whether a program such as this could provide a sustainable model for plague prevention in endemic areas.Item Use of Insecticide Delivery Tubes for Controlling Rodent-Associated Fleas in a Plague Endemic Region of West Nile, Uganda(Journal of medical entomology, 2014) Boegler, Karen A.; Atiku, Linda A.; Tendo Mpanga, Joseph; Clark, Rebecca J.; Delorey, Mark J.; Gage, Kenneth L.; Eisen, Rebecca J.Plague is a primarily flea-borne rodent-associated zoonosis that is often fatal in humans. Our study focused on the plague-endemic West Nile region of Uganda where affordable means for the prevention of human plague are currently lacking. Traditional hut construction and food storage practices hinder rodent exclusion efforts, and emphasize the need for an inexpensive but effective host-targeted approach for controlling fleas within the domestic environment. Here we demonstrate the ability of an insecticide delivery tube that is made from inexpensive locally available materials to reduce fleas on domestic rodents. Unbaited tubes were treated with either an insecticide alone (fipronil) or in conjunction with an insect growth regulator [(S)-methoprene], and placed along natural rodent runways within participant huts. Performance was similar for both treatments throughout the course of the study, and showed significant reductions in the proportion of infested rodents relative to controls for at least 100 d posttreatment.