Field assessment of dog as sentinel animal for plague in endemic foci of Madagascar

The epidemiology of Yersinia pestis, the causative agent of plague, involves vectors and reservoirs in its transmission cycle. The passive plague surveillance in Madagascar targets mainly rodent and fleas. However, carnivores are routinely surveyed as sentinels of local plague activity in some countries. The aim of this study is to assess the use of domestic dog (Canis familiaris) as sentinel animal for field surveillance of plague in a highly endemic area in Madagascar. Cross-sectional surveys of plague antibody prevalence in C. familiaris were conducted in endemic areas with contrasting histories of plague cases in humans, as well as a plague free area. Rodent capture was done in parallel to evaluate evidence for Y. pestis circulation in the primary reservoirs. In 2 sites, dogs were later re-sampled to examine evidence of seroconversion and antibody persistence. Biological samplings were performed between March 2008 and February 2009. Plague antibody detection was assessed using anti-F1 ELISA. Our study showed a significant difference in dog prevalence rates between plague-endemic and plague-free areas, with no seropositive dogs detected in the plague free area. No correlation was found between rodents and dog prevalence rates, with an absence of seropositive rodents in some area where plague circulation was indicated by seropositive dogs. This is consistent with high mortality rates in rodents following infection. Re-sampling dogs identified individuals seropositive on both occasions, indicating high rates of re-exposure and/or persistence of plague antibodies for at least 9 months. Seroconversion or seropositive juvenile dogs indicated recent local plague circulation. In Madagascar, dog surveillance for plague antibody could be useful to identify plague circulation in new areas or quiescent areas within endemic zones. Within active endemic areas, monitoring of dog populations for seroconversion (negative to positive) or seropositive juvenile dogs could be useful for identifying areas at greatest risk of human outbreaks.     

No evidence for enzootic plague within black-tailed prairie dog (Cynomys ludovicianus) populations

Yersinia pestis, causative agent of plague, occurs throughout the western United States in rodent populations and periodically causes epizootics in susceptible species, including black-tailed prairie dogs (Cynomys ludovicianus). How Y. pestis persists long-term in the environment between these epizootics is poorly understood but multiple mechanisms have been proposed, including, among others, a separate enzootic transmission cycle that maintains Y. pestis without involvement of epizootic hosts and persistence of Y. pestis within epizootic host populations without causing high mortality within those populations. We live-trapped and collected fleas from black-tailed prairie dogs and other mammal species from sites with and without black-tailed prairie dogs in 2004 and 2005 and tested all fleas for presence of Y. pestis. Y. pestis was not detected in 2126 fleas collected in 2004 but was detected in 294 fleas collected from multiple sites in 2005, before and during a widespread epizootic that drastically reduced black-tailed prairie dog populations in the affected colonies. Temporal and spatial patterns of Y. pestis occurrence in fleas and genotyping of Y. pestis present in some infected fleas suggest Y. pestis was introduced multiple times from sources outside the study area and once introduced, was dispersed between several sites. We conclude Y. pestis likely was not present in these black-tailed prairie dog colonies prior to epizootic activity in these colonies. Although we did not identify likely enzootic hosts, we found evidence that deer mice (Peromyscus maniculatus) may serve as bridging hosts for Y. pestis between unknown enzootic hosts and black-tailed prairie dogs.     

Use of a public telephone hotline to detect urban plague cases

Current methods for vector‐borne disease surveillance are limited by time and cost. To avoid human infections from emerging zoonotic diseases, it is important that the United States develop cost‐effective surveillance systems for these diseases. This study examines the methodology used in the surveillance of a plague epizootic involving tree squirrels (Sciurus niger) in Denver Colorado, during the summer of 2007. A call‐in centre for the public to report dead squirrels was used to direct animal carcass sampling. Staff used these reports to collect squirrel carcasses for the analysis of Yersinia pestis infection. This sampling protocol was analysed at the census tract level using Poisson regression to determine the relationship between higher call volumes in a census tract and the risk of a carcass in that tract testing positive for plague. Over‐sampling owing to call volume‐directed collection was accounted for by including the number of animals collected as the denominator in the model. The risk of finding an additional plague‐positive animal increased as the call volume per census tract increased. The risk in the census tracts with >3 calls a month was significantly higher than that with three or less calls in a month. For tracts with 4–5 calls, the relative risk (RR) of an additional plague‐positive carcass was 10.08 (95% CI 5.46–18.61); for tracts with 6–8 calls, the RR = 5.20 (2.93–9.20); for tracts with 9–11 calls, the RR = 12.80 (5.85–28.03) and tracts with >11 calls had RR = 35.41 (18.60–67.40). Overall, the call‐in centre directed sampling increased the probability of locating plague‐infected carcasses in the known Denver epizootic. Further studies are needed to determine the effectiveness of this methodology at monitoring large‐scale zoonotic disease occurrence in the absence of a recognized epizootic.     

Identifying the spatiotemporal clusters of plague occurrences in China during the Third Pandemic

Plague, a devastating infectious disease caused by Yersinia pestis, has killed millions of people in the past and is still active in the natural foci of the world today. Understanding the spatiotemporal patterns of plague outbreaks in history is critically important, as it may help to facilitate prevention and control of potential future outbreaks. In this study, we explored spatiotemporal clusters of human plague occurrences in China using a machine‐learning clustering method and reconstructed the potential transmission pattern during the Third Pandemic (1772–1964). We succeeded in identifying 6 clusters in the space domain (2D) and 13 clusters in the spatiotemporal domain (3D). Our results suggest that there were several temporal outbreaks and transmissions of plague in different spatial clusters. Together with the spatiotemporal nearest neighbor approach (ST‐NNA), this method could allow us to have a clearer look at the spatiotemporal patterns of plague.     

From the recent lessons of the Malagasy foci towards a global understanding of the factors involved in plague reemergence

Re-emergence of human cases of plague after decades of silence does not necessarily mean that plague foci are re-emerging. Most often, Yersinia pestis bacteria have been maintained and circulating at low levels in the rodent populations. It seems therefore more appropriate to speak in terms of expansion or regression phases for sylvatic rodent plague foci and to reserve the term re-emergence for human cases. From the analysis of well-documented human plague cases in Madagascar, we underline the causes of re-emergence that can be generalized to most world foci, and can help define environments at risk where the threat of new emergence lurks. In all recent plague outbreaks, usually more than one risk factor was at the origin of the re-emergence. The reduction or discontinuance of surveillance and control, as well as poverty and insalubrity are the main factors in the re-emergence of human cases, allowing increased contacts with infected rodents and fleas. Environment changes (i.e. climatic changes, deforestation, urbanization) induce changes in flea and rodent populations by (i) extension of rodent habitats (for example by replacing forests by steppes or farmlands); (ii) modifications in population dynamics (possible outbreaks due to an increase of available food resources); but also, (iii) emergence of new vectors, reservoirs and new Y. pestis genotypes. Numerous and spontaneous genomic rearrangements occur at high frequencies in Y. pestis, which may confer selective advantages, enhancing the ability of Y. pestis to survive, to be transmitted to new hosts, and to colonize new environments. Therefore, any environmental change should be taken as a warning signal and active surveillance programs should be initiated.     

Yersinia pestis: examining wildlife plague surveillance in China and the USA

Plague is a zoonotic disease caused by the bacterium Yersinia pestis Lehmann and Neumann, 1896. Although it is essentially a disease of rodents, plague can also be transmitted to people. Historically, plague has caused massive morbidity and mortality events in human populations, and has recently been classified as a reemerging disease in many parts of the world. This public health threat has led many countries to set up wild and domestic animal surveillance programs in an attempt to monitor plague activity that could potentially spill over into human populations. Both China and the USA have plague surveillance programs in place, but the disease dynamics differ in each country. We present data on plague seroprevalence in wildlife and review different approaches for plague surveillance in the 2 countries. The need to better comprehend plague dynamics, combined with the fact that there are still several thousand human plague cases per year, make well-designed wildlife surveillance programs a critical part of both understanding plague risks to humans and preventing disease outbreaks in the future.     

Local-scale diversity of Yersinia pestis: A case study from Ambohitromby,Ankazobe District,Madagascar

Plague is a re-emerging zoonotic disease and a major public health concern in several portions of the world, especially in Madagascar. We report on the presence of different subtypes of Yersinia pestis co-occurring in the same locality. After confirmation of a human plague case in Ambohitromby Commune (Ankazobe District) via isolation of Y. pestis, we undertook small mammal trapping to identify the circulation of Y. pestis amongst rodents in this locality; blood samples were collected from rodents for seroprevalence analysis. Of the 60 individuals of Rattus rattus captured, one yielded an isolate of Y. pestis, 13 others were positive for F1 antigen of Y. pestis using a rapid diagnostic test, and 4 were PCR positive targeting the caf1 and pla genes; 28/60 (46.7%) of the captured R. rattus were seropositive for Y. pestis. Whole-genome SNP analyses revealed that the two isolates obtained from the human case, and the R. rattus belonged to two different subtypes of Y. pestis (s05 and s13, respectively) that were circulating concurrently in Ambohitromby in 2016. Three Y. pestis subtypes (s03, s05 and s13) have now been isolated from Ambohitromby. Subtype s05 had been persisting there for >10 years but one or both of the other subtypes may have been introduced from the Central Highlands region as they were not observed in previous years (s13) or only observed once previously (s03). High seroprevalence against Y. pestis in R. rattus suggests that a portion of the local murine population may have acquired resistance to Y. pestis. Future research should focus on genomically characterizing Y. pestis strains circulating in Ankazobe District and other plague-endemic regions of Madagascar to better understand the overall phylogeography of Y. pestis.     

A survey of rats trapped in the wellington area for ectoparasites and organisms of the salmonella,pasteurella, and leptospiral groups

Extract

It has long been established that rats can play an important part in the transference of infectious diseases to man. With this fact in mind, the late Dr J. H. Blakelock, former Director of the National Health Institute, Wellington, began a survey of the rat population in the Wellington district and of rats brought to the area by overseas ships. This work has been continued, the trapped rats being examined for the presence of Xenopsylla cheopis, a flea known to be the chief vector of plague, for Pasteurella pestis, the causative organism of plague, for organisms of the Salmonella group, and for evidence of leptospiral infection.     

Rodent control to fight plague: field assessment of methods based on rat density reduction

Rodents represent a serious threat to food security and public health. The extent to which rodent control can mitigate the risk from rodent-borne disease depends on both the effectiveness of control in reducing rodent abundance and the impact on disease epidemiology. Focusing on a plague-endemic region of Madagascar, this study compared the effectiveness of 3 methods: live-traps, snap-traps, and rodenticides. Control interventions were implemented inside houses between May and October 2019. Tracking tiles monitored rodent abundance. Rodent fleas, the vector involved in plague transmission, were collected. Rodent populations consisted of Rattus rattus and Mus musculus. In terms of trap success, we found that our live-trap regime was more effective than snap-traps. While all 3 control strategies appeared to reduce in-house rodent activity in the short term, we found no evidence of a longer-term effect, with in-house rodent abundance in treated sites comparable to non-treatment sites by the following month. Endemic flea, Synopsyllus fonquerniei, is a key plague vector usually found on rats living outdoors. Although we found no evidence that its abundance inside houses increased following control, this may have been due to a lack of power caused by significant variation in S. fonquerniei abundance. The presence of S. fonquerniei in houses was more likely when S. fonquerniei abundance on outdoor rats was higher, which in turn correlated with high rat abundance. Our results emphasize that control strategies need to consider this connectivity between in-house rat–flea populations and the outdoor populations, and any potential consequences for plague transmission.     

Ocurrence of <Emphasis Type="Italic">Philophthalmus gralli</Emphasis> (Trematoda: Philophthalmidae) in farmed ostriches in Brazil

This paper reports the occurrence of parasitism by the Oriental eye-fluke, Philophthalmus gralli in ostriches reared in a commercial flock from the State of Minas Gerais State, Southeastern Brazil. The two affected birds presented lacrimation, inflammatory reaction and loss of body condition. After physical examination the birds revealed, 17 and 15 trematodes each, only in the right eyes. The economic impact of this parasite on Brazilian ostrich industry is still undetermined, requiring further studies.     

Interrelationship of soil moisture and temperature to sylvatic plague cycle among prairie dogs in the Western United States

Plague, caused by Yersinia pestis, is a flea-borne disease that is endemic in areas throughout the world due to its successful maintenance in a sylvatic cycle, mainly in areas with temperate climates. Burrowing rodents are thought to play a key role in the enzootic maintenance as well as epizootic outbreaks of plague. In the United States, prairie dogs (Cynomys), rodents (Muridae), and ground squirrels (Spermophilus) are susceptible to infection and are parasitized by fleas that transmit plague. In particular, prairie dogs can experience outbreaks that rapidly spread, which can lead to extirpation of colonies. A number of ecological parameters, including climate, are associated with these epizootics. In this study, we asked whether soil parameters, primarily moisture and temperature, are associated with outbreaks of plague in black-tailed prairie dogs and Gunnison's prairie dogs in the Western United States, and at what depth these associations were apparent. We collected publicly available county-level information on the occurrence of population declines or colony extirpation, while historical soil data was collected from SCAN and USCRN stations in counties and states where prairie dogs have been located. The analysis suggests that soil moisture at lower depths correlates with colony die-offs, in addition to temperature near the surface, with key differences within the landscape ecology that impact the occurrence of plague. Overall, the model suggests that the burrow environment may play a significant role in the epizootic spread of disease amongst black-tailed and Gunnison's prairie dogs.     

Puumala Virus Outbreak in Western Thuringia,Germany, 2010: Epidemiology and Strain Identification

In 2010, the highest annual number of human Puumala virus (PUUV) infections was reported in Germany since hantavirus surveillance started in 2001. The increase in annual case numbers was especially marked in western Thuringia. We combined results of case‐based hantavirus surveillance in humans and serological and molecular investigations in the rodent reservoir to describe the epidemiological situation and to identify the putative outbreak strain. A 5‐fold increase in notified hantavirus cases compared to the previous annual maximum was observed in western Thuringia in 2010. Disease incidence varied tremendously within a small geographical area with case patients' places of residence clustering around beech‐dominated broad leaf forest patches. Investigations in the rodent reservoir revealed a novel Puumala virus (PUUV) subtype, which is clearly distinct from strains collected in other PUUV endemic regions of Germany. It can be assumed that in regions in western Thuringia where hantavirus cases occurred in 2010 or previous outbreak years, PUUV has been present in the environment for a long time. Further studies are needed to elucidate the population dynamics and hantavirus prevalence of the rodent reservoir and driving ecological factors.     

Increased detection of rabies virus in bats in Ceará State (Northeast Brazil) after implementation of a passive surveillance programme

The intensification of dog, cat and livestock vaccination campaigns significantly reduced rabies cases in humans and domestic animals in Ceará State, Brazil. However, sylvatic animals—bats (order Chiroptera), wild canids, raccoons and non‐human primates— remain as reservoirs for the virus. Our hypothesis is that surveillance and monitoring of rabies virus in bats, especially passive surveillance, is of fundamental importance, besides the implementation of health education and strengthening of surveillance actions in humans exposed to aggressions. Thus, we assessed the occurrence of rabies virus in animals focusing on bats, before and after launching of the Sylvatic Rabies Surveillance Program in 2010. Surveillance data from the 184 municipalities of Ceará State were analysed, collected during the periods 2003–2010 (active surveillance) and 2011–2016 (passive surveillance), respectively. A total of 13,543 mammalian samples were received for rabies diagnosis from 2003 to 2016. Of these, 10,960 were from dogs or cats (80.9%), 1,180 from bats (8.7%), 806 from other sylvatic animals (foxes, marmosets, raccoons; 6.0%) and 597 from herbivores (cattle, goats, sheep, equines, pigs; 4.4%). A total of 588 (4.3%) samples were positive for rabies. About 8.4% (99/1,180) of the bat samples were infected with rabies virus, 92 (92.9%) of these were from non‐haematophagous bat species and 7 (7.1%) from haematophagous species. The number of bat samples received and infection rates increased considerably, after a shift from active surveillance (9/355 [2.5%] samples positive), to passive surveillance (90/825 [10.9%] samples positive). Surveillance of rabies virus in bats is fundamental for human and domestic animal health in Ceará State. Bats have to be considered as targets in surveillance and control programmes. Virus lineages should be characterized to increase knowledge on transmission dynamics of sylvatic rabies virus to domestic animals and the human population, and to provide additional evidence for planning and implementation of improved control measures.     

Animal disease and public health

Extract

It has been recognized for many centuries that human and animal health are closely related. One of the earliest examples of such recognition which is easily available is from the book of Judges in the Old Testament, where it is reported that the Philistines, after capturing the Ark of the Covenant in a battle with the Israelites, suffered a plague associated with large numbers of rodents and with “emerods”, which we might well believe to be bubos. It seems reasonable to explain this severe epidemic, which apparently killed 50,000 Bethsemites apart from other people, as an example of bubonic plague. Several of the other early accounts of epidemics in which there was an association of large numbers of rats with the occurrence of the disease would appear to be accounts of bubonic plague.     

Cutaneous pythiosis in a dog from Brazil

This report describes a case of cutaneous pythiosis in a 6‐year‐old female mixed breed dog, from the central west region of São Paulo State, Brazil. The cytological and histopathological analyses showed an intense inflammatory infiltrate with presence of numerous hyphal elements, suggesting infection due to Pythium insidiosum. The diagnosis was confirmed by nested‐PCR, which was carried out with specific primers derived from the ribosomal DNA region. The pathogen occurs in Brazil and veterinarians should be aware of the importance of correctly diagnosing this disease and differentiating it from other fungal diseases.     

Non‐human primates as a reservoir for rabies virus in Brazil

Rabies virus (RABV) does not persist in the environment as it is a very fragile agent. The primary hosts are mammalian species in the orders Carnivora and Chiroptera. Since the late 1980s, RABV has been isolated from non‐human primates, Callithrix jacchus (the white‐tufted marmoset), in four coastal states (Rio Grande do Norte, Ceará, Piauí and Pernambuco) in north‐eastern Brazil, where this species is indigenous. The original habitat of C. jacchus consisted of two Brazilian biomes, the Atlantic Forest and the Caatinga. However, these marmosets have since adapted to other ecosystems as a result of human activities. Between 1988 and 1989, RABV isolates were obtained from white‐tufted marmosets in the state of Rio Grande do Norte, but antigenic and genetic identification studies were not conducted at that time. In the following years, three additional states reported cases (Ceará, Piauí and Pernambuco). In two of these states (Ceará and Piauí), human cases of rabies transmitted by marmosets were reported. According to Brazilian Health Ministry data, at least 19 human cases in which this species was the source of infection were registered in between 1990 and 2016. Recent findings in laboratory tests of 12 rabid samples from humans and marmosets and the regional transmission among these animals for over 20 years, together with the gradual increase in the affected geographic area, support the concept of the emergence of a new RABV reservoir. Regional tourism, the wild animal trade and the cultural practice of maintaining these animals as pets, particularly in coastal regions, appear to be major risk factors for the increase in human cases. Additional epidemiological and ecological studies are required to better understand local disease dynamics and to identify ideal opportunities for prevention and control of this fatal infection.     

Brazilian spotted fever: A spatial analysis of human cases and vectors in the state of São Paulo,Brazil

Brazilian spotted fever (BSF) is a highly lethal disease caused by Rickettsia spp. and is transmitted by ticks of the genus Amblyomma. Understanding the epidemiology of BSF in each region can help direct health surveillance actions. The objective of this study was to determine the spatial distribution of vectors and the incidence of BSF in the state of São Paulo. Spatial analysis included confirmed BSF cases between 2009 and 2019; occurrences were registered by municipalities of the state. There were 752 confirmed BSF cases, with incidences ranging between 0.01 and 10.37/10,000 inhabitants. Moran's Global Index for BSF was 0.20 (p = .001), which was indicative of spatial dependence. Moran's map located a cluster of 20 high priority municipalities for BSF and showed that Amblyomma sculptum is the vector involved in Rickettsia rickettsii transmission in these locations. Spatial analysis identified clusters formed by 47, 20 and seven significant municipalities for the presence of A. sculptum, Amblyomma aureolatum and Amblyomma ovale vectors, respectively. Surveillance and prevention actions are necessary in areas that are at high risk for BSF and in areas where the presence of vectors was significant.     

Rabies virus and Histoplasma suramericanum coinfection in a bat from southeastern Brazil

Bats are essential to the global ecosystem, but their ability to harbour a range of pathogens has been widely discussed, as well as their role in the emergence and re‐emergence of infectious diseases. This paper describes the first report of coinfection by two zoonotic agents, rabies virus (RABV) and the fungus Histoplasma suramericanum in a bat. The bat was from the Molossus molossus species, and it was found during the daytime in the hallway of a public psychiatric hospital in a municipality in São Paulo State, southeastern Brazil. RABV infection was diagnosed by the direct fluorescent antibody test and mouse inoculation test. The fungus was isolated by in vitro culture. Both diagnoses were confirmed by molecular techniques. Phylogenetic analysis showed that the fungus isolate had proximity to H. suramericanum in the Lam B clade, while the RABV isolate was characterized in the Lasiurus cinereus lineage. Since the M. molossus bat was found in a peri‐urban transition area (urban/peri‐urban), the possibility of cross‐species transmission of this RABV lineage becomes more plausible, considering that this scenario may provide shelter for both M. molossus and L. cinereus. These are relevant findings since there has been an increase in bat populations in urban and peri‐urban areas, particularly due to environmental modifications and anthropogenic impacts on their habitat. Thus, the detection of two zoonotic agents in a bat found in a public hospital should raise awareness regarding the importance of systematic surveillance actions directed towards bats in urban areas.     

Plasmodium vivax and Plasmodium falciparum infection in Neotropical primates in the western Amazon,Brazil

The Brazilian Amazon is endemic for malaria and natural infections by Plasmodium spp. have been detected in Neotropical primates. Despite the diversity of primate species in the region, studies on infections by these agents are limited. The aim of the present study was to investigate the frequency of infection by Plasmodium vivax and P. falciparum in free‐born primates that were kept in captivity, in the western Amazon, Brazil. Blood samples were collected from 98 Neotropical primates. Detection of P. vivax and P. falciparum DNA was performed using a semi‐nested PCR, and the amplified products were sequenced. Plasmodium spp. DNA was detected in 6.12% (6/98) of the primates. P. vivax, and P. falciparum DNA was detected in 2.04% (2/98) and 4.08% (4/98) of these mammals, respectively. Sequencing and phylogenetic analysis confirmed the results obtained from the semi‐nested PCR. The presence of infected non‐human primates (NHP) can be auxiliary in the maintenance of P. falciparum and P. vivax and may have implications for the malaria surveillance and control in the Brazilian Amazon. It is necessary to structure an efficient surveillance system for the aetiological agents of malaria that infect NHP and humans to reduce the risk of Plasmodium spp. introduction into new areas, to protect all susceptible species.     

Present status of the conservation of livestock genetic resources in Brazil

Brazil has various species of domestic animals, which developed from breeds brought by the Portuguese settlers soon after the discovery of the country. After being submitted to a long process of natural selection, these breeds present characteristics adapted to specific Brazilian environmental conditions, and are known as “criollo”, “local” or naturalized breeds. From the beginning of the 20th century, some exotic breeds, selected in temperate regions, have begun to be imported, and, although more productive, they do not have adaptive traits, such as resistance to disease and parasites found in the naturalized breeds. Even so, they gradually replaced the native breeds, to such an extent that the latter are in danger of extinction. To avoid further loss of this important genetic material, in 1983 the National Research Center for Genetic Resources and Biotechnology (Cenargen) of the Brazilian Agricultural Research Corporation (Embrapa) decided to include conservation of animal genetic resources among its priorities. The conservation activities have been conducted under the Brazilian Genetic Resources Network — Renargen, and is carried out by various research centres of Embrapa, universities and State research institutions, as well as by private farmers, with a single coordinator at national level, Cenargen. The in situ conservation of cattle, horses, buffaloes, donkeys, goats, sheep and pigs is being carried out by Conservation Nuclei, located in the animal's original habitat. Ex situ conservation is centred at the Brazilian Animal Germplasm Bank (AGB), kept at Cenargen. This is responsible for the storage of semen and embryos of various breeds of domestic animals threatened with extinction. Presently the AGB has almost 60,000 doses of semen and more than 250 embryos, as well as over 7000 DNA samples. An important challenge for this program is to increase awareness within the different segments of society in terms of the importance of the conservation of animal genetic resources. The development and evolution of Renargen and its efforts to facilitate the conservation of genetic resources of livestock in Brazil are described in this paper.