Inter-epizootic Periods Research Articles

Epizootic Activity of Natural Plague Foci in the Russian Federation in 2013 and Prognosis for the Year of 2014

Analyzed are the data of the epizootiologic survey of plague enzootic territories in Russia in 2013. Evaluated are the numbers of major carriers and vectors as well as the epizootic activity of natural foci of different types. Analysis of preconditions for decrease of epizootic potential of plague natural foci of Caucasus, Altai and Tyva is carried out. Single findings of infected fleas are registered at the sites of steady focality in the territory of Pre-Caspian lowland. Forecast of epizootic situation for 2014 is presented. Marked is raising probability that Volga-Ural sandy and Central Caucasian high-mountain plague foci would get out of the inter-epizootic period state. Substantiated are the possibility of plague epizootics continuation and their intensity in Pre-Caspian sandy, Altai and Tyva mountain, and Eastern-Caucasus high-mountain plague natural foci.

Epidemiological study of Rift Valley fever virus in Kigoma, Tanzania.

Rift Valley fever virus (RVFV) is an acute, zoonotic viral disease caused by a Phlebovirus, which belongs to the Bunyaviridae family. Among livestock, outbreaks of the disease are economically devastating. They are often characterised by large, sweeping abortion storms and have significant mortality in adult livestock. The aim of the current study was to investigate RVFV infection in the Kigoma region, which is nestled under the hills of the western arm of the Great Rift Valley on the edge of Lake Tanganyika, Tanzania. A region-wide serosurvey was conducted on non-vaccinated small ruminants (sheep and goats, n = 411). Sera samples were tested for the presence of anti-RVFV antibodies and viral antigen, using commercial enzyme-linked immunosorbent assay and reverse transcriptase polymerase chain reaction, respectively. The overall past infections were detected in 22 of the 411 animals, 5.4% (Confidence Interval (CI) 95% = 3.5% - 8.1%). The Kigoma rural area recorded the higher seroprevalence of 12.0% (CI 95% = 7.3% - 18.3%; p < 0.0001), followed by Kibondo at 2.3% (CI 95% = 0.5% - 6.5%; p > 0.05) and the Kasulu district at 0.8% (CI 95% = 0.0% - 4.2%; p > 0.05). The prevalence was 12.5% and 4.7% for sheep and goats, respectively. Reverse transcriptase polymerase chain reaction results indicated that only eight samples were found to be positive (n = 63). This study has confirmed, for the first time, the presence of the RVFV in the Kigoma region four years after the 2007 epizootic in Tanzania. The study further suggests that the virus activity exists during the inter-epizootic period, even in regions with no history of RVFV.

143 Rift Valley fever virus

The capacity of Rift Valley fever virus (RVFV) to spread into new territories by crossing significant natural geographic barriers, re-emerge in endemic regions after long periods of silence to cause large outbreaks in human and animal populations constitute a formidable challenge for public and veterinary health authorities as well as for scientific communities worldwide. In spite of recent advances in research on RVFV pathogenesis, molecular epidemiology, outbreak prediction, development of new diagnostic tools and vaccines, some fundamental aspects of the epidemiology and ecology of the virus remain elusive. Large outbreaks of RVF are associated with anomalous high rainfalls leading to massive flooding and the resultant swarms of competent mosquito vectors transmitting the virus to a wide range of susceptible vertebrate species. However, the exact mechanism of RVFV natural transmission during interepizootic periods remains largely unknown, including the postulated long-term virus persistence in transovarially infected eggs of floodwater Aedes mosquito species, and the role of wild mammals as reservoirs. The presence of competent mosquito vectors in countries free of RVF, the wide range of mammals susceptible to the virus, the global changes in climate, and increased animal trade and travel are some of the factors which might contribute to international spread. This presentation provides the background to the major outbreaks, molecular biology and epidemiology of RVFV, and overviews aspects of ecology, host and vector range which make the virus a potential global emerging threat.

Development of real-time RT-PCR for the detection of low concentrations of Rift Valley fever virus

In recent years, Madagascar and the Comoros archipelago have been affected by epidemics of Rift Valley fever (RVF), however detection of Rift Valley fever virus (RVFV) in zebu, sheep and goats during the post epidemic periods was frequently unsuccessful. Thus, a highly sensitive real-time RT-PCR assay was developed for the detection of RVFV at low viral loads. A new RVF SYBR Green RT-PCR targeting the M segment was tested on serum from different RVF seronegative ruminant species collected from May 2010 to August 2011 in Madagascar and the Comoros archipelago and compared with a RVF specific quantitative real time RT-PCR technique, which is considered as the reference technique. The specificity was tested on a wide range of arboviruses or other viruses giving RVF similar clinical signs. A total of 38 out of 2756 serum samples tested positive with the new RT-PCR, whereas the reference technique only detected 5 out of the 2756. The described RT-PCR is an efficient diagnostic tool for the investigation of enzootic circulation of the RVF virus. It allows the detection of low viral RNA loads adapted for the investigations of reservoirs or specific epidemiological situations such as inter-epizootic periods.

Impact of the Present-Day Climate Changes on the Natural Plague Foci Condition, Situated in the Territory of the Russian Federation and Other CIS Countries

Climate changes determine dynamics of epizootic activity of natural plague foci in the XX and XXI centuries. Obvious shift to continentality in the Northern hemisphere can put an end to inter-epizootic period in lowland steppe and semi-desert natural foci of the Pre-Caucasian region, North and North-West Caspian Sea regions. Presently observed conjoined development of inter-epizootic periods in natural plague foci with different biocoenotic structure in the territory of Pre-Caspian Lowland gives the grounds for assuming the presence of a common cause preconditioning parasitic system depression in the region. One of the key elements of this phenomenon is a change of status of little souslik – formerly the main plague carrier in the region. Subsequent to the climate change the key role of plague carrier is more often played by non-hibernating rodent species nowadays. Thus a significant increase in epizootic potential of steppe natural plague foci in the territory of Kazakhstan and Central Asia is prognosticated. With the further temperature fall during wintertime, snow cover height increase and glacial area extension epizootic activity of the mountain and high mountain foci must drop off significantly. Alongside with this updated data on plague agent ecology, predetermining possibility of its existence in the soil biota, confirm the key role of climactic factors in the plague enzootic outbreak.

Absence of Rift Valley Fever Virus in Wild Small Mammals, Madagascar

Absence of Rift Valley Fever Virus in Wild Small Mammals, Madagascar

Epizootic Activity of Natural Plague Foci in the Russian Federation in 2012 and Prognosis for the Year of 2013

Integrated are the data on the number of major carriers and vectors as well as the epizootic activity of natural foci of plague of different types in the territory of Russia in 2012. Submitted is the short-term forecast of epizootic situation for 2013. Analyzed are the reasons of current low epizootic activity of plain natural foci of plague. The role of climatic factors in the development of long inter-epizootic periods in plague natural foci in the Pre-Caucasus, Pre-Caspian regions and Siberia is discussed. Assessed is the change of potential epidemiologic hazard of plague-enzootic territories under the current warming of climate. The long-term forecast of epizootic activity of natural plague foci for the period of up to 2020 is substantiated.

Rapid assay to differentiate the two forms of Egyptian Aedes caspius (diptera: culicidae) using acetylcholinesterase gene

Abstract Members of Aedes caspius mosquitoes are incriminated to be a potential reservoir of “Rift Valley Fever Virus” (RVF) during interepizootic periods in Egypt. Ae. caspius contains two distinct forms which are morphologically indistinguishable but differ in physiology and behavior; Ae. caspius form (a) requires a blood meal for each egg batch(anautogeny), is unable to mate in confined spaces(eurygamous). The second form (b) lays egg batch without blood meal (autogenous) and can mate in confined spaces (stenogamous). In this work, we collected the autogenous and anautogenous forms of Ae. caspius from two different breeding habitats in the Qalyubia Governorate. Analysis of the Drosophila ace-Orthologous acetylecholinesterase gene revealed that a single polymorphic region characterized each species. Based on this region, specific primers were used to amplify the entire section of intron II, sections of Exon 2 and Exon 3 of ace-2 gene for differentiating the complex species of mosquitoes. The amplicons of anautogenous form sized 441 pb and increase 116 bp than autogenous form of Ae. caspius. High rates of point mutations were addressed; deletion/insertion events are 120 bases. The transversion mutations were 44 bases and were relatively close to the transtion mutations 43 base. The genetic distance was 0.01 between the two forms.

Local persistence and extinction of plague in a metapopulation of great gerbil burrows, Kazakhstan

Speculation on how the bacterium Yersinia pestis re-emerges after years of absence in the Prebalkhash region in Kazakhstan has been ongoing for half a century, but the mechanism is still unclear. One of the theories is that plague persists in its reservoir host (the great gerbil) in so-called hotspots, i.e. small regions in which the conditions remain favourable for plague to persist during times where the conditions in the Prebalkhash region as a whole have become unfavourable for plague persistence. In this paper we use a metapopulation model that describes the dynamics of the great gerbil. With this model we study the minimum size of an individual hotspot and the combined size of multiple hotspots in the Prebalkhash region that would be required for Y. pestis to persist through an inter-epizootic period. We show that the combined area of hotspots required for plague persistence is so large that it would be unlikely to have been missed by existing plague surveillance. This suggests that persistence of plague in that region cannot solely be explained by the existence of hotspots, and therefore other hypotheses, such as survival in multiple host species, and persistence in fleas or in the soil should be considered as well.

Evaluation of the Infectiousness to Mice of Soil Contaminated with Yersinia pestis-Infected Blood

Plague, an often-fatal zoonotic disease caused by Yersinia pestis, is characterized by epizootic and quiescent periods. How Y. pestis is maintained during inter-epizootic periods is poorly understood, but soil has been implicated as a potential reservoir. Although previous studies have suggested that Y. pestis is able to survive in soil for weeks or months, it is unclear whether or not it is infectious to susceptible hosts. Here we investigate the potential for Y. pestis to infect mice through close contact with contaminated soil under laboratory conditions. In an attempt to approximate the natural conditions under which animals would be exposed to Y. pestis-contaminated soil, mouse cages filled with soil from a plague-endemic region were held at temperature and humidity ranges observed in ground squirrel burrows. These laboratory "burrows" were contaminated with highly bacteremic blood (>10(8) cfu/mL) to simulate the introduction of infectious material from a dying animal during an epizootic. Outbred Swiss-Webster mice with scarified skin patches were held on contaminated soil for 10 days and monitored for signs of illness. Following exposure to contaminated soil, one animal of 104 became infected with Y. pestis. None of the remaining animals seroconverted following a 21-day holding period. Under our experimental conditions, which maximized the likelihood of contact between susceptible mice and contaminated soil, transmission efficiency from soil to mice was 0.96% (95% CI 0.17, 5.25%). This suggests that although transmission of Y. pestis from contaminated soils is possible, it is not likely a major transmission route under natural conditions.

Recovery and molecular characterization of live Camelpox virus from skin 12 months after onset of clinical signs reveals possible mechanism of virus persistence in herds

Potentially pathogenic orthopoxviruses (OPVs) persist in nature and re-emerge for reasons we do not fully understand. New information pertaining to Orthopoxvirus (OPV) persistence in nature would significantly improve surveillance and control programs. In a recent investigation of a Camelpox virus (CMLV) outbreak in Eastern Saudi Arabia, atypical minute pox-like skin lesions (AMPL) persisted on 42.9% of convalescent camels (8.8% of herd) for more than a year after the onset of clinical signs. In order to investigate whether AMPL were related to CMLV infection, AMPL homogenates were inoculated on the chorioallantoic membranes (CAM) of specific-pathogen-free (SPF) embryonating chicken eggs (ECE). Live CMLV was recovered from AMPL homogenates. The sequences of the ATIP gene of viruses isolated in the beginning of the outbreak, and one year later from AMPL were identical, and similar to the Kazakhstan isolate CMLV M-96. Virus identity was confirmed by sequence analysis of the CMLV A33R, A27L, B5R, and L1R orthologue genes. Uninfected adult camels that came in contact with animals showing AMPL became infected within two weeks. Since AMPL were easily missed by veterinarians and camel drivers, it was concluded that CMLV survival in persistent skin lesions may be a key mechanism in maintaining the virus in previously infected camel herds during inter-epizootic periods.

Flea Diversity as an Element for Persistence of Plague Bacteria in an East African Plague Focus

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 inter-epizootic 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.

Epizootic of dolphin morbillivirus on the Catalonian Mediterranean coast in 2007

BETWEEN 1990 and 1992, thousands of striped dolphins ( Stenella coeruleoalba ) stranded along the Mediterranean coast due to a newly described virus, the dolphin morbillivirus (DMV) (Domingo and others...

Investigation of the Ecology ofFrancisella tularensisDuring an Inter-Epizootic Period

A 1-year study of the ecological cycle of Francisella tularensis was performed in an enzootic area during an inter-epizootic period. The study was based on multiple sampling of all major constituents of the disease cycle. Seroprevalence of tularemia in the European brown hare (Lepus europaeus) population was 5.1% (10/197) with low antibody titers (1/10 and 1/20), and F. tularensis ssp. holarctica was isolated from four hares. F. tularensis was not detected in the 38 common voles (Microtus arvalis), 110 yellow-necked mice (Apodemus flavicollis), or 15 stripped field mice (Apodemus agrarius) trapped during the study, or the by-catch of 8 Eurasian pygmy shrews (Sorex minutus) or 6 common shrews (Sorex araneus). A total of 1106 Ixodes ricinus and 476 Haemaphysalis concinna ticks were collected from vegetation, and 404 I. ricinus, 28 H. concinna ticks, and 15 Ctenophtalmus assimilis and 10 Nosopsyllus fasciatus fleas were combed off small mammals. One H. concinna female and one nymph collected from the vegetation was found infected with F. tularensis ssp. holarctica by TaqMan polymerase chain reaction, thus resulting a 0.42% (2/476) prevalence. F. tularensis-specific DNA was not detected in environmental water samples, and the examined 100 sheep, 50 cows, and 50 buffalos grazed at the study area were all seronegative. During inter-epizootic periods, F. tularensis ssp. holarctica seems to persist only in the European brown hare--H. concinna cycle at the studied habitat. H. concinna may not serve exclusively as an arthropod vector, but it may also harbor bacteria for 3-4 years through multiple life stages and act as an important reservoir of F. tularensis. Rodent species probably do not serve as true reservoir hosts of tularemia.

Susceptibility of the Common Hamster (Cricetus cricetus) to Francisella tularensis and Its Effect on the Epizootiology of Tularemia in an Area Where Both Are Endemic

Francisella tularensis is a highly infectious zoonotic agent causing the disease tularemia. The common hamster (Cricetus cricetus) is considered a pest in eastern Europe, and believed to be a source of human tularemia infections. We examined the role of the common hamster in the natural cycle of tularemia using serologic methods on 900 hamsters and real-time polymerase chain reaction (PCR) on 100 hamsters in an endemic agricultural area. We collected 374 Ixodes acuminatus ticks from the hamsters and tested them by real-time PCR. All tests were negative. To examine clinical signs, pathology, and histopathology of acute tularemia infection similar to the natural infection, two hamsters were infected with a large dose of a wild strain of F. tularensis ssp. holarctica. After a short period of apathy, the animals died on the eighth and ninth days postinfection. The pathologic, histopathologic, and immunohistochemical examination contributed to the diagnosis of septicemia in both cases. Our results confirmed previous findings that common hamsters are highly sensitive to F. tularensis. We conclude that although septicemic hamsters may pose substantial risk to humans during tularemia outbreaks, hamsters in interepizootic periods do not act as a main reservoir of F. tularensis.

Rift Valley fever in Kenya: history of epizootics and identification of vulnerable districts

Since Kenya first reported Rift Valley fever (RVF)-like disease in livestock in 1912, the country has reported the most frequent epizootics of RVF disease. To determine the pattern of disease spread across the country after its introduction in 1912, and to identify regions vulnerable to the periodic epizootics, annual livestock disease records at the Department of Veterinary Services from 1910 to 2007 were analysed in order to document the number and location of RVF-infected livestock herds. A total of 38/69 (55%) administrative districts in the country had reported RVF epizootics by the end of 2007. During the 1912-1950 period, the disease was confined to a district in Rift Valley province that is prone to flooding and where livestock were raised in proximity with wildlife. Between 1951 and 2007, 11 national RVF epizootics were recorded with an average inter-epizootic period of 3·6 years (range 1-7 years); in addition, all epizootics occurred in years when the average annual rainfall increased by more than 50% in the affected districts. Whereas the first two national epizootics in 1951 and 1955 were confined to eight districts in the Rift Valley province, there was a sustained epizootic between 1961 and 1964 that spread the virus to over 30% of the districts across six out of eight provinces. The Western and Nyanza provinces, located on the southwestern region of the country, had never reported RVF infections by 2007. The probability of a district being involved in a national epizootic was fivefold higher (62%) in districts that had previously reported disease compared to districts that had no prior disease activity (11%). These findings suggests that once introduced into certain permissive ecologies, the RVF virus becomes enzootic, making the region vulnerable to periodic epizootics that were probably precipitated by amplification of resident virus associated with heavy rainfall and flooding.

Identification of potential vectors of and detection of antibodies against Rift Valley fever virus in livestock during interepizootic periods

To evaluate the prevalence of Rift Valley fever virus (RVFV) antibodies in livestock and presence of competent mosquito vectors of RVFV during an interepizootic period (IEP) in Kenya. 208 sheep and 84 goats ranging in age from 4 months to 15 years, from 2 breeding herds. Blood specimens were collected from the sheep and goats during the 1999-2006 IEP in Rift Valley Province, and serum was harvested. Serum specimens were tested for IgG and IgM antibodies against RVFV by use of an ELISA. In addition, 7,134 mosquitoes were trapped in Naivasha, Nairobi, and Northeastern Province, and speciation was performed. No animals were seropositive for IgM against RVFV. Of the animals born after the 1997-1998 epizootic, 18% (34/188) of sheep were seropositive for IgG against RVFV, compared with 3% (2/75) of goats. Seventy percent (8,144/11,678) of the mosquitoes collected were of the Culex subgenera; 18% (2,102/11,678) were Aedes spp. Detection of IgG in the sera of sheep and goats born after the 1997-1998 epizootic and before the 2006 epizootic indicated that virus activity existed during the IEP. Detection of Aedes mosquitoes, which are competent vectors of RVFV, suggested that a cryptic vector-to-vertebrate cycle may exist during IEPs.

Vector Control Improves Survival of Three Species of Prairie Dogs (Cynomys) in Areas Considered Enzootic for Plague

Plague causes periodic epizootics that decimate populations of prairie dogs (PDs) (Cynomys), but the means by which the causative bacterium (Yersinia pestis) persists between epizootics are poorly understood. Plague epizootics in PDs might arise as the result of introductions of Y. pestis from sources outside PD colonies. However, it remains possible that plague persists in PDs during interepizootic periods and is transmitted at low rates among highly susceptible individuals within and between their colonies. If this is true, application of vector control to reduce flea numbers might reduce mortality among PDs. To test whether vector control enhances PD survival in the absence of obvious plague epizootics, we reduced the numbers of fleas (vectors for Y. pestis) 96-98% (1 month posttreatment) on 15 areas involving three species of PDs (Cynomys leucurus, Cynomys parvidens in Utah, and Cynomys ludovicianus in Montana) during 2000-2004 using deltamethrin dust delivered into burrows as a pulicide. Even during years without epizootic plague, PD survival rates at dusted sites were 31-45% higher for adults and 2-34% higher for juveniles compared to survival rates at nondusted sites. Y. pestis was cultured from 49 of the 851 flea pools tested (6882 total fleas) and antibodies against Y. pestis were identified in serum samples from 40 of 2631 PDs. Although other explanations are possible, including transmission of other potentially fatal pathogens by fleas, ticks, or other ectoparasites, our results suggest that plague might be maintained indefinitely in PD populations in the absence of free epizootics and widespread mortality among these animals. If PDs and their fleas support enzootic cycles of plague transmission, there would be important implications for the conservation of these animals and other species.

Flea Diversity and Infestation Prevalence on Rodents in a Plague-Endemic Region of Uganda

In Uganda, the West Nile region is the primary epidemiologic focus for plague. The aims of this study were to 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, Rattus rattus, 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.

Adaptive strategies of Yersinia pestis to persist during inter-epizootic and epizootic periods.

Plague is a flea-borne zoonotic bacterial disease caused by Yersinia pestis. It has caused three historical pandemics, including the Black Death which killed nearly a third of Europe's population in the 14th century. In modern times, plague epizootics can extirpate entire susceptible wildlife populations and then disappear for long time periods. Understanding how Y. pestis is maintained during inter-epizootic periods and the factors responsible for transitioning to epizootics is important for preventing and controlling pathogen transmission and ultimately reducing the burden of human disease. In this review, we focus primarily on plague in North American foci and discuss the potential adaptive strategies Y. pestis might employ to ensure not only its survival during inter-epizootic periods but also the rapid epizootic spread and invasion of new territories that are so characteristic of plague and have resulted in major pandemics and establishment of plague foci throughout much of the world.