ArticleLiterature Review

The Significant but Understudied Impact of Pathogen Transmission from Humans to Animals

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Abstract

Zooanthroponotic pathogens, which are transmitted from humans to nonhuman animals, are an understudied aspect of global health, despite their potential to cause significant disease burden in wild and domestic animal populations and affect global economies. Some key human-borne pathogens that have been shown to infect animals and cause morbidity and mortality include measles virus (paramyxoviruses), influenza A virus (orthomyxoviruses), herpes simplex 1 virus (herpesviruses), protozoal and helminthic parasites, and bacteria such as methicillin-resistant Staphylococcus aureus and Mycobacterium tuberculosis. However, zooanthroponotic pathogens are most commonly reported in captive animals or domestic livestock with close human contact; there, the potential for economic loss and human reinfection is most apparent. There is also the potential for infection in wild animal populations, which may threaten endangered species and decrease biodiversity. The emergence and reemergence of human-borne pathogens in wildlife may also have negative consequences for human health if these pathogens cycle back into humans. Many of the anthropogenic drivers of zoonotic disease emergence also facilitate zooanthroponotic transmission. Increasing research to better understand the occurrence of and the potential for bidirectional pathogen transmission between humans and animals is essential for improving global health. Mt Sinai J Med 76:448–455, 2009. © 2009 Mount Sinai School of Medicine

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... Genetic similarity between humans and apes may increase the likelihood of being more susceptible to the same pathogens 6,8 . In some cases, nonhuman primates may experience higher morbidity and mortality when infected with common human pathogens 9 . ...
... Many of the same anthropogenic activities that cause zoonotic diseases to emerge in human populations, such as deforestation, agricultural intensification, hunting, ecotourism and even scientific research, have also increasingly brought people and apes into contact 6,[13][14][15][16][17] . Zooanthroponotic transmission (transmission of disease from people to animals) of viral and bacterial pathogens to apes have had severe impacts on ape health 9 . Two common human respiratory pathogens: human metapneumovirus and human respiratory syncycial virus, were found to be the cause of fatal disease in chimpanzees in the Tai Forest, Cote D'Ivoire 3 and Tanzania 18 . ...
Research
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This report collates data collected through a systematic literature review and an expert opinion survey to estimate the risk of releasing a gibbon or an orangutan infected with certain etiological agents into a potentially naïve population of wild apes. A thorough risk assessment was conducted by combining these methods. We identified potential health hazards through the literature review and used the results from the expert opinion survey to develop stoplight hazard assessments for gibbons (Hylobatidae) and Bornean orangutans (P. pygmaeus). We present these results with the recommended surveillance and monitoring activities for apes in Sabah, but could likely be applied in all of Borneo. A monitoring and surveillance plan can play a key role in the assessment and risk management of infectious diseases. It can provide baseline prevalence data, be used to estimate population health risks of releasing rehabilitated or translocated apes, determine when an outbreak is occurring and produce descriptive epidemiological data on etiological agents. The surveillance plan detailed here is designed to improve the health of wild, rehabilitated and captive apes.
... Influenza A virus (IAV), an enveloped virus with segmented, negative single-strand RNA linear genome, is one of the most serious pathogens in the world, causing significantly negative impacts on economy and human-animal health (Epstein & Price, 2009). Based on its surface antigens, IAV was classified into different subtypes related to the antigenic characteristics of hemagglutinin (HA) and neuraminidase [1]. ...
... To date, 18 types of HA (H1 -H18) and 11 type of NA (N1 -N11) were identified [2], among which the last two HA and NA subtypes tended to be specific to bats [3]. Subtypes H1N1 and H3N2 currently spread throughout the human population [4][5][6][7]. Similarly, H5, H7, and H9 still cause serious problem in poultry production as evidenced by high mortality rate and loss of egg production. ...
Article
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Influenza A virus is one of the most serious diseases in the world. Therefore, it is necessary to find an effective and safe method to prevent the spread of the disease. A far-UVC at 222nm is considered safe and effective for viral and bacterial treatment. In this study, virucidal effects and the safety status of far-UVC microplasma were evaluated in vitro against influenza A virus H9N2 0130 strain. The results (from TCID 50 and real-time PCR) indicated that a far-UVC inhibited influenza A virus depending on dosage. A far-UVC eliminated 99.99% of the virus at doses of 44 and 56 mJ/cm 2 in clarified and un-clarified solutions, respectively. Moreover, a far-UVC 222 nm did not have any harmful effects in MDCK cell at dose 78 mJ/cm 2. Our study provided useful information in a far-UVC application against influenza A virus.
... In addition to ecotourists, researchers or poachers form an additional source of viruses. Mainly in areas where anthropozoonotic transmission is likely to occur, the necessary resources to identify outbreaks and their causative agents are often absent [46], limiting the possibility for interrupting outbreaks. Since potential MV transmission from human to NHP could lead to a large measles outbreak with high mortality rates in endangered ape species, vaccination against measles of free-ranging NHP populations in areas frequently visited by ecotourists could be warranted [46]. ...
... Mainly in areas where anthropozoonotic transmission is likely to occur, the necessary resources to identify outbreaks and their causative agents are often absent [46], limiting the possibility for interrupting outbreaks. Since potential MV transmission from human to NHP could lead to a large measles outbreak with high mortality rates in endangered ape species, vaccination against measles of free-ranging NHP populations in areas frequently visited by ecotourists could be warranted [46]. ...
Chapter
Non-human primates (NHP) have played a crucial rule in the history of morbillivirus research. Although NHPs are naturally susceptible to morbillivirus infections, outbreaks are rare among monkeys and apes living in their natural habitat. However, introduction of a highly contagious morbillivirus in a high-density population or captive colony seronegative for morbilliviruses can easily lead to an efficient transmission chain in which all animals become infected. Secondary infections due to morbillivirus-induced immune suppression can subsequently yield complications, leading to outbreaks with high morbidity and mortality. In this chapter, we provide an overview of morbillivirus outbreaks that have occurred in different monkey species, and we discuss morbillivirus epidemiology in different target species. Furthermore, differences in infection course and severity in various species are discussed. In addition to discussing natural infection of NHP with morbilliviruses, this chapter provides an overview of experimental infections of NHP with wildtype or genetically engineered morbilliviruses. These studies have contributed significantly to a more complete understanding of measles pathogenesis.
... Moreover, humans populate all continents and many islands, and hence are considered ubiquitous across ecosystems; some authors even claim that there are absolutely no ecosystems free of anthropization (Sanderson et al., 2002). So, it is a fact that humans are in direct and indirect contact with wild animals, thus humans are a hazard for wildlife because of their potential for pathogen transmission (Epstein and Price, 2009). In fact, there are previous virus spillover records from human to animals (v. ...
... gr. measles, human metapneumovirus, human respiratory syncytial virus and herpes simplex virus type 1; Epstein and Price, 2009), including human coronavirus transmitted from humans to pigs in China (Chen et al., 2005) and from humans to chimpanzees (Pan troglodytes verus) in Ivory Coast (Patrono et al., 2018). Since human-influence/humanfootprint occurs across all world ecosystems (Sanderson et al., 2002), the interaction with wild animals is almost impossible to avoid. ...
Article
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Severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) can infect animals, however, the whole range of potential hosts is still unknown. This work makes an assessment of wildlife susceptibility to SARS-CoV-2 by analyzing the similarities of Angiotensin Converting Enzyme 2 (ACE2) and Transmembrane Protease, Serine 2 (TMPRSS2) —both recognized as receptors and protease for coronavirus spike protein— and the genetic variation of the viral protein spike in the recognition sites. The sequences from different mammals, birds, reptiles, and amphibians, and the sequence from SARS-CoV-2 S protein were obtained from the GenBank. Comparisons of aligned sequences were made by selecting amino acids residues of ACE2, TMPRSS2 and S protein; phylogenetic trees were reconstructed using the same sequences. The species susceptibility was ranked by substituting the values of amino acid residues for both proteins. Our results ranked primates at the top, but surprisingly, just below are carnivores, cetaceans and wild rodents, showing a relatively high potential risk, as opposed to lab rodents that are typically mammals at lower risk. Most of the sequences from birds, reptiles and amphibians occupied the lowest ranges in the analyses. Models and phylogenetic trees outputs showed the species that are more prone to getting infected with SARS-CoV-2. Interestingly, during this short pandemic period, a high haplotypic variation was observed in the RBD of the viral S protein, suggesting new risks for other hosts. Our findings are consistent with other published results reporting laboratory and natural infections in different species. Finally, urgent measures of wildlife monitoring are needed regarding SARS-CoV-2, as well as measures for avoiding or limiting human contact with wildlife, and precautionary measures to protect wildlife workers and researchers; monitoring disposal of waste and sewage than can potentially affect the environment, and designing protocols for dealing with the outbreak.
... Scientists have long recognized the risk of pathogen spillover from humans to bats [94][95][96], but bat researchers in North America have not systematically addressed this risk prior to WNS. Outside of reservoir host studies, few bat researchers studied infectious diseases in bats before WNS emerged in 2007 [73] nor studied bat viruses (other than rabies) before bats were retrospectively connected to the SARS epidemic [15,66,97]. ...
... Conservation-compatible surveillance of bat viruses has demonstrated the potential for mutually beneficial collaboration between public health scientists and conservation stakeholders [94,113,125,128,129]. Disease-focused studies that integrate ecological principles into a rigorous study design provide the most informative context to interpret bat-virus associations and patterns of richness globally [130][131][132]. ...
Article
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The COVID-19 pandemic highlights the substantial public health, economic, and societal consequences of virus spillover from a wildlife reservoir. Widespread human transmission of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) also presents a new set of challenges when considering viral spillover from people to naïve wildlife and other animal populations. The establishment of new wildlife reservoirs for SARS-CoV-2 would further complicate public health control measures and could lead to wildlife health and conservation impacts. Given the likely bat origin of SARS-CoV-2 and related beta-coronaviruses (β-CoVs), free-ranging bats are a key group of concern for spillover from humans back to wildlife. Here, we review the diversity and natural host range of β-CoVs in bats and examine the risk of humans inadvertently infecting free-ranging bats with SARS-CoV-2. Our review of the global distribution and host range of β-CoV evolutionary lineages suggests that 40+ species of temperate-zone North American bats could be immunologically naïve and susceptible to infection by SARS-CoV-2. We highlight an urgent need to proactively connect the wellbeing of human and wildlife health during the current pandemic and to implement new tools to continue wildlife research while avoiding potentially severe health and conservation impacts of SARS-CoV-2 "spilling back" into free-ranging bat populations.
... The public health threat is apparent, with approximately 60% of emerging infectious diseases resulting from zoonotic transmission, but negative consequences of disease emergence are not unique to humans. Numerous examples exist of disease spillover from humans and domestic animals into wildlife, with long-term and devastating consequences (Cleaveland et al., 2005;Epstein & Price, 2009;Kock et al., 1999;Michel et al., 2009;Nituch, Bowman, Beauclerc, & Schulte-Hostedde, 2011;Nugent, 2011;Roelke-Parker et al., 1996). ...
... Primates are recognized as an important taxon in emerging disease events, given close phylogenetic relatedness to humans, serving as sentinels and sources of infections in humans, while themselves suffering from human-associated pathogens (Calvignac-Spencer, Leendertz, Gillespie, & Leendertz, 2012;Epstein & Price, 2009;Jones et al., 2008;Wolfe, Dunavan, & Diamond, 2007;Woolhouse & Gowtage-Sequeria, 2005). Primates, particularly great apes, have also gained growing conservation interest. ...
Article
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Syndromic surveillance is an incipient approach to early wildlife disease detection. Consequently, systematic assessments are needed for methodology validation in wildlife populations. We evaluated the sensitivity of a syndromic surveillance protocol for respiratory disease detection among chimpanzees in Gombe National Park, Tanzania. Empirical health, behavioural, and demographic data were integrated with an agent‐based, network model to simulate disease transmission and surveillance. Surveillance sensitivity was estimated as 66% (95% CI: 63.1, 68.8%) and 59.5% (95% CI: 56.5%, 62.4%) for two monitoring methods (weekly count and prevalence thresholds respectively), but differences among calendar quarters in outbreak size and surveillance sensitivity suggest seasonal effects. We determined that a weekly detection threshold of ≥2 chimpanzees with clinical respiratory disease leading to outbreak response protocols (enhanced observation and biological sampling) is an optimal algorithm for outbreak detection in this population. Synthesis and applications. This is the first quantitative assessment of syndromic surveillance in wildlife, providing a model approach to detecting disease emergence. Coupling syndromic surveillance with targeted diagnostic sampling in the midst of suspected outbreaks will provide a powerful system for detecting disease transmission and understanding population impacts.
... Zoonotic pathogens account for approximately 75% of emerging infectious diseases (EID) in humans , with spillover from wildlife to humans having been identified as one of the primary threats to global health (Jones et al., 2008;Epstein and Price, 2009). As a result, emerging zoonoses are increasingly being recognised as playing a fundamental role in determining community health (John, 2013). ...
... One still largely unexplored aspect of global heath is the potential transmission of human-borne pathogens to wildlife and domestic animals (zooanthroponosis) (Epstein and Price, 2009). Infections with zoonotic protozoan parasites, such as Cryptosporidium, Giardia and Toxoplasma (Current and Garcia, 1991;Dubey, 2009;) are known to be responsible for high levels of disease and morbidity in humans, but these zoonotic pathogens also infect wild and domestic animals . ...
... So the entire herd was treated. Considering the zoonotic importance of the disease, the zoo keepers and the persons closely associated with the herd ware kept under screening for any possible infection of that organism [5,6]. ...
... Nimba found no difference in relative estimates provided by direct observations and camera traps(van Leeuwen et al., 2020). The use of camera traps, rather than direct observations, also has several additional benefits, including reduced potential for transmission of anthroponotic diseases to the apes(Epstein & Price, 2009), less unintended behavioral change (McDougall, 2012), and potentially a reduced vulnerability to poaching in some communities (Robbins & Boesch, 2019) depending on the nature of local threats. ...
Article
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Primate social organizations, or grouping patterns, vary significantly across species. Behavioral strategies that allow for flexibility in grouping patterns offer a means to reduce the costs of group living. Chimpanzees ( Pan troglodytes ) have a fission‐fusion social system in which temporary subgroups (“parties”) change in composition because of local socio‐ecological conditions. Notably, western chimpanzees ( P. t. verus ) are described as showing a higher degree of bisexual bonding and association than eastern chimpanzees, and eastern female chimpanzees ( P. t. schweinfurthii ) are thought to be more solitary than western female chimpanzees. However, reported comparisons in sociality currently depend on a small number of study groups, particularly in western chimpanzees, and variation in methods. The inclusion of additional communities and direct comparison using the same methods are essential to assess whether reported subspecies differences in sociality hold in this behaviorally heterogeneous species. We explored whether sociality differs between two communities of chimpanzees using the same motion‐triggered camera technology and definitions of social measures. We compare party size and composition (party type, sex ratio) between the western Gahtoy community in the Nimba Mountains (Guinea) and the eastern Waibira community in the Budongo Forest (Uganda). Once potential competition for resources such as food and mating opportunities were controlled for, subspecies did not substantially influence the number of individuals in a party. We found a higher sex‐ratio, indicating more males in a party, in Waibira; this pattern was driven by a greater likelihood in Gahtoy to be in all‐female parties. This finding is the opposite of what was expected for eastern chimpanzees, where female‐only parties are predicted to be more common. Our results highlight the flexibility in chimpanzee sociality, and caution against subspecies level generalizations.
... Influenza is one of the best known examples of bidirectional transmission between humans and domestic pigs (12). The emergence and re-emergence of these pathogens has important implications for human and animal health (13). This risk appears to be even greater when bidirectional transmission between humans and animals is frequent, as in the case of TB in elephants (14). ...
Article
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Introduction Tuberculosis is an infectious disease caused by a group of acid-fast bacilli known as Mycobacterium tuberculosis complex (MTC), which has a major impact on humans. Transmission of MTC across the human-animal interface has been demonstrated by several studies. However, the reverse zoonotic transmission from humans to animals (zooanthroponosis) has often been neglected. Methods In this study, we used Nanopore MinION and Illumina MiSeq approaches to sequence the whole genome of M. tuberculosis strains isolated from two deceased Asian elephants (Elephas maximus) and one human in Chitwan, Nepal. The evolutionary relationships and drug resistance capacity of these strains were assessed using the whole genome data generated by the stand-alone tool Tb-Profiler. Phylogenomic trees were also constructed using a non-synonymous SNP alignment of 2,596 bp, including 94 whole genome sequences representative of the previously described M. tuberculosis lineages from elephants worldwide (lineages 1 and 4) and from humans in Nepal (lineages 1, 2 and 3). Results and Discussion The new genomes achieved an average coverage of 99.6%, with an average depth of 55.67x. These M. tuberculosis strains belong to lineage 1 (elephant DG), lineage 2 (elephant PK) and lineage 4 (human), and none of them were found to have drug-resistant variants. The elephant-derived isolates were evolutionarily closely related to human-derived isolates previously described in Nepal, both in lineages 1 and 2, providing additional support for zooanthroponosis or bidirectional transmission between humans and elephants. The human-derived isolate clustered together with other published human isolates from Argentina, Russia and the United Kingdom in the lineage 4 clade. This complex multi-pathogen, multi-host system is challenging and highlights the need for a One Health approach to tuberculosis prevention and control at human-animal interface, particularly in regions where human tuberculosis is highly endemic.
... In addition to their increasing prevalence and incidence, MRSA infections are associated with rising morbidity and mortality, in comparison to methicillin-susceptible S. aureus (MSSA) infections [10,32,33]. Furthermore, the bacterium has the ability to switch host [29,[34][35][36] even after long periods of isolation in a single host species [37]. ...
Article
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Although antibiotic resistance is a major issue for both human and animal health, very few studies have investigated the role of the bacterial host spectrum in its dissemination within natural ecosystems. Here, we assessed the prevalence of methicillin resistance among Staphylococcus aureus (MRSA) isolates from humans, non-human primates (NHPs), micromammals and bats in a primatology center located in southeast Gabon, and evaluated the plausibility of four main predictions regarding the acquisition of antibiotic resistance in this ecosystem. MRSA strain prevalence was much higher in exposed species (i.e., humans and NHPs which receive antibiotic treatment) than in unexposed species (micromammals and bats), and in NHP species living in enclosures than those in captivity-supporting the assumption that antibiotic pressure is a risk factor in the acquisition of MRSA that is reinforced by the irregularity of drug treatment. In the two unexposed groups of species, resistance prevalence was high in the generalist strains that infect humans or NHPs, supporting the hypothesis that MRSA strains diffuse to wild species through interspecific transmission of a generalist strain. Strikingly, the generalist strains that were not found in humans showed a higher proportion of MRSA strains than specialist strains, suggesting that generalist strains present a greater potential for the acquisition of antibiotic resistance than specialist strains. The host spectrum is thus a major component of the issue of antibiotic resistance in ecosystems where humans apply strong antibiotic pressure.
... The presence of lymphadenopathy in MPXV is a striking clinical feature that distinguishes it from smallpox [21]. MPXV can be transmitted from monkeys and terrestrial rodents [22]. According to the first report in 1958, monkeys and other susceptible animals were infected with MPXV only in the tropical rain forests of Central and West Africa. ...
Article
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Non-human primates (NHP) share a close relationship with humans due to a genetic homology of 75–98.5%. NHP and humans have highly similar tissue structures, immunity, physiology, and metabolism and thus often can act as hosts to the same pathogens. Agriculture, meat consumption habits, tourism development, religious beliefs, and biological research have led to more extensive and frequent contact between NHPs and humans. Deadly viruses, such as rabies virus, herpes B virus, Marburg virus, Ebola virus, human immunodeficiency virus, and monkeypox virus can be transferred from NHP to humans. Similarly, herpes simplex virus, influenza virus, and yellow fever virus can be transmitted to NHP from humans. Infectious pathogens, including viruses, bacteria, and parasites, can affect the health of both primates and humans. A vast number of NHP-carrying pathogens exhibit a risk of transmission to humans. Therefore, zoonotic infectious diseases should be evaluated in future research. This article reviews the research evidence, diagnostic methods, prevention, and treatment measures that may be useful in limiting the spread of several common viral pathogens via NHP and providing ideas for preventing zoonotic diseases with epidemic potential.
... The specific epidemiological risks manifested consequently in factory farms are fivefold. First, factory farms focus on productivity intensification, whereby they present an extensive, homogenous host population that is concentrated in a limited space and increasing the potential for viral transmission [15,44]. Second, factory farms may crowd together animal populations from multiple species, thus creating conditions for viral mutations that are more transmissible to humans; the lack of ventilation and sunlight increases the virus survival, enabling the potential and susceptibility of immunosuppressed animals to become infected [45]. ...
Article
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Infectious diseases are rooted in unsustainable and unjust human–animal relationships. Zoonoses are facilitated by human proximity to animals, epidemiological risk embedded within factory farms, and exploitation of animals and humans in these intensive livestock production systems. The five major categories of epidemiological risk that factory farms propel include: intensification of production for which homogenous populations are congregated, creation of multi-species farms for which different animals are held within the same farm, long and intensive animal transport increases the likelihood of interaction with other wildlife, ecological characteristics of the pathogen lead to altered pathogen dynamics and antibiotic resistance within a human population through the overuse of antibiotics. Layer and broiler operations in the North American context illustrate these linkages. One Health is offered as a concluding conceptual and aspirational frame for pursuing a more sustainable and just world. This article offers two main messages. First, our relationships with animals directly impact the health of human populations through the transmission and creation of Emerging Infectious Diseases (EIDs). Second, adopting One Health offers a means forward for more just and sustainable human–animal relations and reduction of zoonoses transmission.
... Transmission of human pathogens to non-human animals, including wildlife, occurs more regularly than often thought [18,19]. SARS-CoV-2 appears to have a striking ability to infect a broad range of distantly related mammals. ...
Article
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Due to marine mammals’ demonstrated susceptibility to SARS-CoV-2, based upon the homology level of their angiotensin-converting enzyme 2 (ACE2) viral receptor with the human one, alongside the global SARS-CoV-2 occurrence and fecal contamination of the river and marine ecosystems, SARS-CoV-2 infection may be plausibly expected to occur also in cetaceans, with special emphasis on inshore species like bottlenose dolphins (Tursiops truncatus). Moreover, based on immune and inflammatory responses to SARS-CoV-2 infection in humans, macrophages could also play an important role in antiviral defense mechanisms. In order to provide a more in-depth insight into SARS-CoV-2 susceptibility in marine mammals, we evaluated the presence of SARS-CoV-2 and the expression of ACE2 and the pan-macrophage marker CD68. Aliquots of tissue samples, belonging to cetaceans stranded along the Italian coastline during 2020–2021, were collected for SARS-CoV-2 analysis by real-time PCR (RT-PCRT) (N =43) and Immunohistochemistry (IHC) (N = 59); thirty-two aliquots of pulmonary tissue sample (N = 17 Tursiops truncatus, N = 15 Stenella coeruleoalba) available at the Mediterranean Marine Mammal Tissue Bank (MMMTB) of the University of Padua (Legnaro, Padua, Italy) were analyzed to investigate ACE2 expression by IHC. In addition, ACE2 and CD68 were also investigated by Double-Labeling Immunofluorescence (IF) Confocal Laser Microscopy. No SARS-CoV-2 positivity was found in samples analyzed for the survey while ACE2 protein was detected in the lower respiratory tract albeit heterogeneously for age, gender/sex, and specie, suggesting that ACE2 expression can vary between different lung regions and among individuals. Finally, double IF analysis showed elevated colocalization of ACE2 and CD68 in macrophages only when an evident inflammatory reaction was present, such as in human SARS-CoV-2 infection.
... When the tamarins crossed on the road, people approached individuals to take pictures and to attempt to offer food. In this sense, the canopy bridge can also decrease the likelihood of direct contact between people and wildlife, and then avoid exchange of pathogens (Epstein and Price 2009), and even decrease the probability of an illegal capture for pet trade; these topics are actually never discussed in the scientific literature related to the benefits of canopy bridges and would deserve attention. ...
Article
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Canopy bridges are crossing structures specific to mitigate the impact of roads on arboreal animals. Long-term monitoring of such infrastructures together with the analysis of design preferences has never been done in South America. To avoid the roadkills of a threatened primate species, the black lion tamarin (Leontopithecus chrysopygus), in Guareí, São Paulo, Brazil, we installed two designs of canopy bridges: a wood pole bridge and a rope bridge. We aimed to (1) evaluate the functionality (number of species and events) of both designs, (2) test the design preference of each species, and (3) determine if there were seasonal differences in the use of canopy bridges. We monitored the canopy bridges continuously since their installation with camera traps during 3 years. We recorded nine mammal and one lizard species crossing on the canopy bridges as well as 13 bird species using them as perches. Overall, the probability of crossing was higher on the wood pole bridge and the number of crossings, considering both designs, was higher during the dry season. One lizard and seven mammal species used the wood pole bridge, including the black lion tamarin, and six mammal species used the rope bridge. Four out of five species tested, including the black lion tamarin, preferred the wood pole bridge. While replications of this experimental design are necessary to obtain a more robust evaluation of the effectiveness of these canopy bridges, our study suggests that wood pole bridges might be an effective tool to reduce roadkills of the endangered black lion tamarin and possibly other arboreal species.
... On the other hand, the use of saliva as a diagnostic sample is advantageous since the virus is readily detected within, it can be easily provided by the patient [53], and it does not require specialized personnel for its collection. In addition, the collection procedure is significantly more comfortable and less invasive than a nasopharyngeal swab or sputum procedure [54]. Many are attempting to develop new diagnostic testing solutions which allow rapid diagnosis of COVID-19 via alternative methods, including blood, sputum, and oropharyngeal secretions [27], but there are currently very few studies regarding the possible role of saliva in the detection of SARS-CoV-2. ...
Article
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Most of people will be infected with a coronavirus at least once in their life, which might be a worrying fact for many people. Coronaviruses are a widespread virus species known to cause diseases ranging from common colds to more severe illnesses. Coronaviruses are of animal origin, which means they are transmitted between animals and humans. However, several known types of coronavirus circulating among animals have not infected humans to date. SARS-CoV-2 is thought to have been transmitted from seafood and animal markets in China to humans. Saliva plays a prominent role in lubricating the alimentary tract bolus, buffering and repairing the oral mucosa, protecting against microorganisms, and other oral functions. Several viruses and bacteria infect the tissue of salivary glands in a specific manner. Saliva is a complicated fluid that plays a crucial role in preventing viral infection, especially through the innate immune system, which is the first line of defense. For example, hyposalivation can result in severe respiratory infection. However, the salivary gland is also a significant reservoir of viruses in saliva, and the live virus can be cultivated from saliva samples. This suggests that asymptomatic spread of SARS-CoV-2 may come from contaminated saliva. The present review summarizes the role of saliva as a reservoir of several viruses in spreading infection and the extent of saliva use in detecting SARSCoV-2 to control the COVID-19 pandemic.
... Airborne transmission and direct contact are modes of reverse zoonotic disease transmission (Epstein & Price, 2009). However, infection through fomites and the environment could also occur as has been suggested by other ape researchers (Gilardi et al., 2005). ...
Article
Respiratory illnesses, including COVID‐19, present a serious threat to endangered wild chimpanzee (Pan troglodytes) populations. In some parts of sub‐Saharan Africa, chimpanzee tracking is a popular tourism activity, offering visitors a chance to view apes in their natural habitats. Chimpanzee tourism is an important source of revenue and thus benefits conservation; however, chimpanzee tracking may also increase the risk of disease transmission from people to chimpanzees directly (e.g., via aerosol transmission) or indirectly (e.g., through the environment or via fomites). This study assessed how tourist behaviors might facilitate respiratory disease transmission at a chimpanzee tracking site in Kibale National Park, Uganda. We observed tourists, guides, and student interns from the time they entered the forest to view the chimpanzees until they left the forest and noted behaviors related to disease transmission. Common behaviors included coughing, sneezing, and urinating, which respectively occurred during 88.1%, 65.4%, and 36.6% of excursions. Per excursion, individuals touched their faces an average of 125.84 ± 34.45 times and touched large tree trunks or branches (which chimpanzees might subsequently touch) an average of 230.14 ± 108.66 times. These results show that many pathways exist by which pathogens might move from humans to chimpanzees in the context of tourism. Guidelines for minimizing the risk of such transmission should consider tourist behavior and the full range of modes by which pathogen transmission might occur between tourists and chimpanzees. Highlights Great ape tourism presents risk for reverse zoonotic infection. Future guidelines for great ape tourism should take into consideration the behavioral propensities of individual tourists.
... Transmission of human pathogens to non-human animals, including wildlife, occurs more regularly than often thought (Epstein & Price 2009, Messenger et al. 2014). SARS-CoV-2 appears to have a striking ability to infect a broad range of distantly related mammals. ...
Article
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It has been a long time since the world has experienced a pandemic with such a rapid devastating impact as the current COVID-19 pandemic. The causative agent, severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2), is unusual in that it appears capable of infecting many different mammal species. As a significant proportion of people worldwide are infected with SARS-CoV-2 and may spread the infection unknowingly before symptoms occur or without any symptoms ever occurring, there is a non-negligible risk of humans spreading SARS-CoV-2 to wildlife, in particular to wild non-human mammals. Because of SARS-CoV-2's apparent evolutionary origins in bats and reports of humans transmitting the virus to pets and zoo animals, regulations for the prevention of human-to-animal transmission have so far focused mostly on these animal groups. We summarise recent studies and reports that show that a wide range of distantly related mammals are likely to be susceptible to SARS-CoV-2, and that susceptibility or resistance to the virus is, in general, not predictable, or only predictable to some extent, from phylogenetic proximity to known susceptible or resistant hosts. In the absence of solid evidence on the susceptibility and resistance to SARS-CoV-2 for each of the >6500 mammal species, we argue that sanitary precautions should be taken by humans interacting with any other mammal species in the wild. Preventing human-to-wildlife SARS-CoV-2 transmission is important to protect these animals (some of which are classed as threatened) from disease, but also to avoid establishment of novel SARS-CoV-2 reservoirs in wild mammals. The risk of repeated re-infection of humans from such a wildlife reservoir could severely hamper SARS-CoV-2 control efforts. Activities during which direct or indirect interaction with wild mammals may occur include wildlife research, conservation activities, forestry work, pest control, management of feral populations, ecological consultancy work, management of protected areas and natural environments, wildlife tourism and wildlife rehabilitation in animal shelters. During such activities, we recommend sanitary precautions, such as physical distancing, wearing face masks and gloves, and frequent decontamination, which are very similar to regulations currently imposed to prevent transmission among humans. We further recommend active surveillance of domestic and feral animals that could act as SARS‐CoV‐2 intermediate hosts between humans and wild mammals.
... Transmission of human pathogens to non-human animals, including wildlife, occurs more regularly than often thought [7,8]. SARS-CoV-2 appears to have a striking ability to infect a broad range of distantly related mammals. ...
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It has been a long time since the world has experienced a pandemic with such a rapid devastating impact as the current COVID-19 pandemic. The causative agent, the Severe Acute Respiratory Syndrome coronavirus 2 (SARS-CoV-2) is further unusual in that it appears capable of infecting many different mammal species. As a significant proportion of people worldwide are infected with SARS-CoV-2 and may spread the infection unknowingly before symptoms occur or without any symptoms ever occurring, there is a non-negligible risk of humans spreading SARS-CoV-2 to wildlife, in particular mammals. Because of SARS-CoV-2’s evolutionary origins in bats and reports of humans transmitting the virus to pets and zoo animals, regulations for prevention of human-to-animal transmission have so far focused mostly on these animal groups. Here, we summarize recent studies and reports that show that a wide range of distantly related mammals are likely susceptible to SARS-CoV-2 and that susceptibility or resistance to the virus is in general not predictable, or only to some extent, by phylogenetic proximity to known susceptible or resistant hosts. In the absence of solid evidence on the SARS-CoV-2 susceptibility/resistance for each of the >5,500 mammal species, we argue that sanitary precautions should be taken when interacting with any mammal species in the wild. Preventing human-to-wildlife SARS-CoV-2 transmission is important for protecting these (sometimes endangered) animals from disease, but also to avoid establishment of novel SARS-CoV-2 reservoirs in wild animals. The risk of repeated re-infection of humans from such a wildlife reservoir could severely hamper SARS-CoV-2 control efforts. For wildlife fieldworkers interacting directly or indirectly with mammals, we recommend sanitary precautions such as physical distancing, wearing face masks and gloves, and frequent decontamination, which are very similar to regulations currently imposed to prevent transmission among humans.
... The long history of co-existence between humans and the apes and frequent contact with neighbouring communities for trade would suggest a range of encounters for potential disease transmission despite a poor historical record regarding the nature and frequency of such encounters (Gagneux et al., 2001). For example, the present evidence suggests that bushmeat hunting has contributed to increasing the risk of paramyxoviruses, such as measles, from humans to both gorillas and chimpanzees (Epstein & Price, 2009;Wolfe, Daszak, Kilpatrick, & Burke, 2005). Measles is estimated to have emerged in the human population between the 11 th and 12 th centuries in the Middle East where people were in proximity to cattle (Furuse, Suzuki, & Oshitani, 2010) and was known to cause widespread devastation on first contact. ...
Thesis
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In this thesis, I examine the complex entanglements among humans, Cross River gorillas (Gorilla gorilla diehli) and Nigeria-Cameroon chimpanzees (Pan troglodytes ellioti) within the unprotected Mone-Oku Forest, Cameroon. I apply a dual ethnoprimatological and political ecology framework to examine the multifaced interconnections between humans and primates that approaches the Mone-Oku landscape as a combination of social, political and ecological systems. I aim to step away from the ‘crisis’ conservation narrative that labels the local people as the largest threat to these endangered apes and strive for a reflexive ethnographic ethnoprimatology. Through a combined use of botanical surveys, analyses of nesting sites, participant observation and semi-structured interviews, I obtained nuanced ecological and ethnographic insight into the human-ape interface. I found that the chimpanzees and gorillas selected distinct nesting ranges within the Mone-Oku Forest. Plant species preferences in the construction of night nests were also observed for both taxa. Anthropogenic activities within the forest, therefore, have different impacts on the nesting behaviour of the apes. Through ethnography and semi-structured interviews, the importance of cacao (Theobroma cacao) to people quickly became apparent. This was reflected in perceptions that held the Mone-Oku Forest to be more important than the individual species within. In contrast, local perceptions of the apes were often contradictory and context dependant ranging from fear to tolerance, some of which stems from power imbalances with conservation organisations. A reconsideration of the conservation narratives for these apes found them to be incomplete and potentially biased, as they neglect some aspects of human-ape interactions, wider community ecology and the microscales of time. This research highlights the complexity of human, gorilla and chimpanzee intra-actions at a specific site. While perfect solutions to conservation problems are not always possible, conservation programs that acknowledge the importance of cocoa and incorporate the variety of knowledge about cacao farming have the potential to foster positive relationships with these communities, furthering the conservation of these endangered apes.
... Most commonly we examine this with wildlife as a reservoir and humans as the affected species (e.g., Ebola, Nipah, MERS, SARS). However, transmission may also occur in reverse, with humans seeding wildlife with pathogens [86,87]. In the case of S. aureus, it appears both may be occurring, as has been previously documented among livestock [9]. ...
Article
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Staphylococcus aureus is a common bacterial colonizer of humans and a variety of animal species. Many strains have zoonotic potential, moving between humans and animals, including livestock, pets, and wildlife. We examined publications reporting on S. aureus presence in a variety of wildlife species in order to more cohesively review distribution of strains and antibiotic resistance in wildlife. Fifty-one studies were included in the final qualitative synthesis. The most common types documented included ST398, ST425, ST1, ST133, ST130, and ST15. A mix of methicillin-resistant and methicillin-susceptible strains were noted. A number of molecular types were identified that were likely to be found in wildlife species, including those that are commonly found in humans or other animal species (including livestock). Additional research should include follow-up in geographic areas that are under-sampled in this study, which is dominated by European studies.
... Despite host-virus specificity, zoonotic transmission has been identified by cross-infection where there is a close genetic relationship between certain human and animal rotaviruses (Brugere-Picoux & Tessier, 2010). The potential for cross-species transmission of viral pathogens, in general, exists where humans and non-human primates (NHP) come into contact and has been documented between humans and several species of NHP in a variety of contexts and in diverse geographic areas (Epstein & Price, 2009;Jones-Engel et al., 2008;Schillaci et al., 2005). ...
Article
Group A rotavirus (RVA) is an important cause of diarrhea in people, especially children, and animals globally. Due to the segmented nature of the RVA genome, animal RVA strains have the potential to adapt to the human host through re‐assortment with other co‐infecting human viruses. Macaques share food and habitat with people, resulting in close interaction between these two species. This study aimed to detect and characterize RVA in rhesus macaques (Macaca mulatta) in Bangladesh. Fecal samples (N = 454) were collected from apparently healthy rhesus macaques from nine different sites in Bangladesh between February and March 2013. The samples were tested by one‐step, real‐time, reverse transcriptase polymerase chain reaction (PCR). Four percent of samples (N = 20; 95% CI 2.7%–6.7%) were positive for RVA. RVA positive samples were further characterized by nucleotide sequence analysis of two structural protein gene fragments, VP4 (P genotype), and VP7 (G genotype). G3, G10, P[3] and P[15] genotypes were identified and were associated as G3P[3], G3P[15] and G10P[15]. The phylogenetic relationship between macaque RVA strains from this study and previously reported human strains indicates possible transmission between humans and macaques in Bangladesh. To our knowledge this is the first report of detection and characterization of rotaviruses in rhesus macaques in Bangladesh. These data will not only aid in identifying viral sharing between macaques, human and other animals, but will also improve the development of mitigation measures for the prevention of future rotavirus outbreaks.
... Regarding pathogens that pass from humans to NHP (named reverse zoonotic disease transmission) and are capable to infect a variable diversity of hosts (also named wide host plasticity) (113)(114)(115), it can be hypothesized that bidirectional transmission (pathogen passed back from NHP to humans) (116), is likely to occur. For example, this could be the case for fecal bacteria repeatedly ingested by different hosts or pathogens transmitted by a blood-feeding insect. ...
Article
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Most of the human pandemics reported to date can be classified as zoonoses. Among these, there is a long history of infectious diseases that have spread from non-human primates (NHP) to humans. For millennia, indigenous groups that depend on wildlife for their survival were exposed to the risk of NHP pathogens' transmission through animal hunting and wild meat consumption. Usually, exposure is of no consequence or is limited to mild infections. In rare situations, it can be more severe or even become a real public health concern. Since the emergence of acquired immune deficiency syndrome (AIDS), nobody can ignore that an emerging infectious diseases (EID) might spread from NHP into the human population. In large parts of Central Africa and Asia, wildlife remains the primary source of meat and income for millions of people living in rural areas. However, in the past few decades the risk of exposure to an NHP pathogen has taken on a new dimension. Unprecedented breaking down of natural barriers between NHP and humans has increased exposure to health risks for a much larger population, including people living in urban areas. There are several reasons for this: (i) due to road development and massive destruction of ecosystems for agricultural needs, wildlife and humans come into contact more frequently; (ii) due to ecological awareness, many long distance travelers are in search of wildlife discovery, with a particular fascination for African great apes; (iii) due to the attraction for ancient temples and mystical practices, others travelers visit Asian places colonized by NHP. In each case, there is a risk of pathogen transmission through a bite or another route of infection. Beside the individual risk of contracting a pathogen, there is also the possibility of starting a new pandemic. This article reviews the known cases of NHP pathogens' transmission to humans whether they are hunters, travelers, ecotourists, veterinarians, or scientists working on NHP. Although pathogen transmission is supposed to be a rare outcome, Rabies virus, Herpes B virus, Monkeypox virus, Ebola virus, or Yellow fever virus infections are of greater concern and require quick countermeasures from public health professionals.
... The use of camera traps is very convenient to overcome this difficulty. 47 It is an important tool that allows studying primates without exacerbating potential threats to the species like the transmission of zoonotic diseases, [48][49][50] and the potential exposure to poachers. 51 While also mitigating the negative impacts of habituation, the use of camera traps can overcome the limitations of direct observations by filming in accessible areas 52,53 and rare or elusive individuals without the potential human presence bias 54,55 ; in a relatively short period of time 47 ...
Article
Background Primate populations are in decline, mainly affected by agriculture leading to habitat loss, fragmentation but also chemical pollution. Kibale National Park (Uganda), Sebitoli forest, surrounded by tea and crop fields, is the home range of chimpanzees presenting congenital facial dysplasia. This study aimed to identify to what extent the same phenotypical features are observed in baboons (Papio anubis) of this area. Methods A total of 25 390 clips recorded by 14 camera traps between January 2017 and April 2018 were analyzed. Results We identified 30 immature and adult baboons of both sexes with nose and lip deformities. They were more frequently observed in the northwestern part of the area. Conclusions A possible effect of pesticides used in crops at the border of their habitat is suspected to alter the embryonic development. This study emphasizes the importance of non‐invasive methods to detect health problems in wild primates that can act as sentinels for human health.
... Human and animal Nipah virus infections have occurred through the consumption of food contaminated by bat excreta [123,124], and greater human exposures to hantavirus through environmental infectious stages followed the growth of rodent populations that exploit agricultural crops [54,55]. Zooanthroponoses ( pathogens transmitted from humans to other animals) are less appreciated, but affect wildlife globally [125,126]. The preponderance of environmentally and vector-transmitted pathogens at the human -wildlife interface raises important challenges to recognize links with resource provisioning. ...
Article
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Human-provided resource subsidies for wildlife are diverse, common and have profound consequences for wildlife–pathogen interactions, as demonstrated by papers in this themed issue spanning empirical, theoretical and management perspectives from a range of study systems. Contributions cut across scales of organization, from the within-host dynamics of immune function, to population-level impacts on parasite transmission, to landscape- and regional-scale patterns of infection. In this concluding paper, we identify common threads and key findings from author contributions, including the consequences of resource subsidies for (i) host immunity; (ii) animal aggregation and contact rates; (iii) host movement and landscape-level infection patterns; and (iv) interspecific contacts and cross-species transmission. Exciting avenues for future work include studies that integrate mechanistic modelling and empirical approaches to better explore cross-scale processes, and experimental manipulations of food resources to quantify host and pathogen responses. Work is also needed to examine evolutionary responses to provisioning, and ask how diet-altered changes to the host microbiome influence infection processes. Given the massive public health and conservation implications of anthropogenic resource shifts, we end by underscoring the need for practical recommendations to manage supplemental feeding practices, limit human–wildlife conflicts over shared food resources and reduce cross-species transmission risks, including to humans. This article is part of the theme issue ‘Anthropogenic resource subsidies and host–parasite dynamics in wildlife’.
... Although the widespread use of antimicrobials among equine species in the U.S. has been addressed in multiple forums, the epidemiology of antimicrobial resistance in bacteria found in horses has not been assessed [2]. Identifying and describing the burden of antimicrobial resistance among domestic species has become even more important due to evidence of potential cross transmission of certain bacteria between humans and domestic species [5]. Both the Centers for Disease Control and Prevention (CDC) and the United States Department of Agriculture (USDA) have reported such findings in past years [6,7]. ...
Article
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Abstract Background Antimicrobial resistance limits traditional treatment options and increases costs. It is therefore important to estimate the magnitude of the problem so as to provide empirical data to guide control efforts. The aim of this study was to investigate the burden and patterns of antimicrobial resistance (AMR) among equine Staphylococcus samples submitted to the University of Kentucky Veterinary Diagnostic Laboratory (UKVDL) from 1993 to 2009. Retrospective data of 1711 equine Staphylococcus samples submitted to the UKVDL during the time period 1993 to 2009 were included in the study. Antimicrobial susceptibility testing, that included 16 drugs, were performed using cultures followed by the Kirby-Bauer disk diffusion susceptibility test. The proportion of resistant isolates by animal breed, species of organism, sample source, and time period were computed. Chi-square and Cochran-Armitage trend tests were used to identify significant associations and temporal trends, respectively. Logistic regression models were used to investigate predictors of AMR and multidrug resistance (MDR). Results A total of 66.3% of the isolates were resistant to at least one antimicrobial, most of which were Staphylococcus aureus (77.1%), while 25.0% were MDR. The highest level of resistance was to penicillins (52.9%). Among drug classes, isolates had the highest rate of AMR to at least one type of β-lactams (49.2%), followed by aminoglycosides (30.2%). Significant (p
... Elephants in zoological collections around the world have been diagnosed with TB (Lewerin et al., 2005;Mikota et al., 2001;Vogelnest, Hulst, Thompson, Lyashchenko, & Herrin, 2015;Zlot et al., 2015), primarily caused by M. tb or, more rarely, Mycobacterium bovis (Mikota & Maslow, 2011). Infections with zoonotic pathogens transmitted from humans to animals (reverse zoonosis or zooanthroponosis) are more frequently reported in captive animals than their wild counterparts (Epstein & Price, 2009). A case of TB caused by M. tb has been documented in a wild African elephant in Kenya, and, although the source of that animal's infection could not be definitively traced, it had known extended prior contact with humans (Obanda et al., 2013). ...
Article
Transfrontier conservation areas represent an international effort to encourage conservation and sustainable development. Their success faces a number of challenges, including disease management in wildlife, livestock and humans. Tuberculosis (TB) affects humans and a multitude of non-human animal species and is of particular concern in sub-Saharan Africa. The Kavango-Zambezi Transfrontier Conservation Area encompasses five countries, including Zimbabwe, and is home to the largest contiguous population of free-ranging elephants in Africa. Elephants are known to be susceptible to TB; thus, understanding TB status, exposure and transmission risks to and from elephants in this area is of interest for both conservation and human health. To assess risk factors for TB seroprevalence, a questionnaire was used to collect data regarding elephant management at four ecotourism facilities offering elephant-back tourist rides in the Victoria Falls area of Zimbabwe. Thirty-five working African elephants were screened for Mycobacterium tuberculosis complex antibodies using the ElephantTB Stat-Pak and the DPP VetTB Assay for elephants. Six of 35 elephants (17.1%) were seropositive. The risk factor most important for seropositive status was time in captivity. This is the first study to assess TB seroprevalence and risk factors in working African elephants in their home range. Our findings will provide a foundation to develop guidelines to protect the health of captive and free-ranging elephants in the southern African context, as well as elephant handlers through simple interventions. Minimizing exposure through shared feed with other wildlife, routine TB testing of elephant handlers and regular serological screening of elephants are recommended as preventive measures.
... With the expansion of urban centers and the use of natural areas for agriculture or livestock breeding, native forest areas have been gradually fragmented, affecting ecosystems (Grisotti 2010). Ecological disturbances create an imbalance in parasite-wildlife cycles, reaching humans in areas next to forest fragments (Epstein and Price 2009). In this context, wild animals play an important role in the urban transmission of vector-borne zoonoses, maintaining parasite transmission cycles (de Almeida Curi et al. 2014). ...
Article
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Trypanosoma cruzi and Leishmania sp. are important protozoan parasites for humans and animals in the Americas, causing Chagas disease and cutaneous or visceral leishmaniasis, respectively. These vector-borne diseases affect permanent and transient populations in developing tropical countries that exhibit favorable conditions for the perpetuation of the parasite cycle. Our objective was to investigate the occurrence of infection with these parasites in wild animals from urban rainforest fragments in the city of Salvador, the largest city in the northeast region of Brazil. Sixty-five wild animals were captured, clinically examined, and sampled for parasite detection by PCR and culture. Ten different mammalian genera were identified, being 58% (38/65) marsupials. The prevalence of T. cruzi and Leishmania sp. infections was 13% and 43%, respectively. Both parasites were detected by PCR in 11% (7/65), three of which were also double infected as determined by culture. Among the 28 animals found infected with at least one parasite (43%, 28/65), 68% (19/28) were marsupials, two specimens were Callithrix sp. (7%), and one was Trinomys sp. (3%). Most infected animals (89%) had no clinical signs of disease. We found that healthy free-living animals from urban rainforest fragments harbored pathogenic trypanosomatids and should be included in epidemiology studies of diseases in big cities in tropical countries, as these cities grow and engulf rainforest remnants.
... We first searched our entire dataset and removed any clear instances of transmission from humans to primates, for example, including records from zoological parks and wildlife rehabilitation centres (as previously noted). We then additionally removed several human viruses most commonly transmitted from humans back to non-human primates to create a subset of data without the most common reverse zoonotic viruses (adeno-associated virus-2; human adenovirus D; human herpesvirus 4; human metapneumovirus; human respiratory syncytial virus; measles virus; mumps virus) 34,35 . We present these additional analyses excluding reverse zoonoses and associated code at http://doi.org/10.5281/zenodo.596810. ...
Article
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The majority of human emerging infectious diseases are zoonotic, with viruses that originate in wild mammals of particular concern (for example, HIV, Ebola and SARS). Understanding patterns of viral diversity in wildlife and determinants of successful cross-species transmission, or spillover, are therefore key goals for pandemic surveillance programs. However, few analytical tools exist to identify which host species are likely to harbour the next human virus, or which viruses can cross species boundaries. Here we conduct a comprehensive analysis of mammalian host-virus relationships and show that both the total number of viruses that infect a given species and the proportion likely to be zoonotic are predictable. After controlling for research effort, the proportion of zoonotic viruses per species is predicted by phylogenetic relatedness to humans, host taxonomy and human population within a species range-which may reflect human-wildlife contact. We demonstrate that bats harbour a significantly higher proportion of zoonotic viruses than all other mammalian orders. We also identify the taxa and geographic regions with the largest estimated number of 'missing viruses' and 'missing zoonoses' and therefore of highest value for future surveillance. We then show that phylogenetic host breadth and other viral traits are significant predictors of zoonotic potential, providing a novel framework to assess if a newly discovered mammalian virus could infect people.
... Tuberculosis mainly affects wild animals if they are exposed to humans and their civilization (Griffith, 1928;Epstein and Price, 2009). The risk of contracting human tuberculosis, in particular, is assumed to be highest in zoological collections in metropolitan areas, for example in the NZG. ...
... The results of these studies suggest that humans impact macaques in several ways. For example, humans can transmit infectious agents to macaques (Epstein and Price 2009 ;Muehlenbein et al. 2010 ). Additionally, people can physically harm macaques. ...
Chapter
Long-tailed macaques commonly live near human settlements in Southeast Asia and Singapore is one example of such an interface. In 2011 and 2012, we conducted a census for Singapore’s National Parks Board (NParks), during which we collected behavioral, demographic, and ranging data. We used these data to examine how the presence of humans and access to human food related to changes in the macaques’ time budget, ranging behavior, and group size. We found that human presence was associated with decreased traveling rates, decreased arboreality, increased terrestriality, and increased use of human-made substrates. In particular, access to human food was associated with larger macaque group sizes, decreased arboreality, and increased use of human-made structures. Our results demonstrate how living near humans in an intensely urban habitat impacts macaques. Perhaps with better knowledge of how humans affect urban macaques, we can better plan management strategies to mitigate conflict. We discuss some nonlethal strategies for managing Singapore’s human–macaque interface that could potentially reduce human–macaque conflict. Specifically, we recommend consistent enforcement of an existing feeding ban, the employment of security guards to mitigate conflict in particularly problematic areas, and the expansion of existing education programs for local people and tourists.
... Although human populations are a demonstrated source of pathogen exchange for NHPs (Epstein & Price 2009), our data imply that habitat disturbance and anthropogenic contact may differently affect the dynamics of parasite infection and disease transmission for different NHP species. Specifically, the ability of vervets and several other Old World primates (e.g. ...
Article
A growing focus of nonhuman primate conservation and management planning concerns factors affecting the dynamics of parasite infection and disease transmission. Here, we examine the effects of anthropogenic and environmental components of the landscape on the prevalence, richness, and species diversity of gastrointestinal parasites in wild-caught vervet monkeys (Chlorocebus aethiops) in South Africa. Nematodes of the genus Trichuris and the family Strongylidae and protists of the subclass Coccidia were present in 55.13% of sampled animals (n = 43). Parasitological, geographical, demographic and climatic correlates of infection were assessed in a geographical information systems (GIS) platform. The findings of this study suggest that parasitism in South African vervets may be better predicted by environmental factors than by degree of anthropogenic contact. This research represents one of the first surveys of parasitic infection in a wild monkey species in southern Africa.
... The frequency of interactions between humans, domestic animals and wildlife is increased by the anthropogenic loss of wildlife habitat which augments the risk of these groups being exposed to novel pathogens (Daszak et al. 2000;Epstein and Price 2009). Many studies have focused on zoonotic diseases originating from wildlife but relatively few have concerned anthroponoses (otherwise known as reverse zoonoses), where human pathogens adversely affect captive or wild animals (Messenger et al. 2014). ...
Article
Streptococcus pyogenes, a common pathogen of humans, was isolated from the carcass of a free-living European hedgehog (Erinaceus europaeus) found in northern England in June 2014. The animal had abscessation of the deep right cervical lymph node, mesenteric lymph nodes and liver. The S. pyogenes strain isolated from the lesions, peritoneal and pleural cavities was characterised as emm 28, which can be associated with invasive disease in humans. This is the first known report of S. pyogenes in a hedgehog and in any free-living wild animal that has been confirmed by gene sequencing. As close associations between wild hedgehogs and people in England are common, we hypothesise that this case might have resulted from anthroponotic infection.
... Tuberculosis mainly affects wild animals if they are exposed to humans and their civilization (Griffith, 1928;Epstein and Price, 2009). The risk of contracting human tuberculosis, in particular, is assumed to be highest in zoological collections in metropolitan areas, for example in the NZG. ...
Article
Full-text available
This study reports on an investigation of Mycobacterium tuberculosis cases in mostly captive wild animals using molecular typing tools [Variable Number of Tandem Repeat (VNTR) typing and Restriction Fragment Length Polymorphism typing]. The investigation included cases from (i) the National Zoological Gardens of South Africa (NZG) recorded between 2002 and 2011; (ii) Johannesburg Zoo, where tuberculosis was first diagnosed in 2007 and has since been detected in three antelope species; (iii) a rehabilitation centre for vervet monkeys (Chlorocebus pygerythrus) in which M. tuberculosis was diagnosed in 2008; and (iv) incidental cases in other facilities including a sable antelope (Hippotragus niger), two unrelated cases in chacma baboons (Papio ursinus) (one of which was from a free-ranging troop) and a colony of capuchin monkeys (Cebus capucinus). Identical genetic profiles of the latter three isolates indicate the persistence of a single M. tuberculosis strain in this population since at least 2006. Results of the outbreak investigation in the captive vervet monkey colony indicate that it was caused by two unrelated strains, while all 13 M. tuberculosis isolates from 11 animal species in the NZG showed different VNTR patterns. A substantial increase in tuberculosis cases of 60% was recorded in the NZG, compared with the previous reporting period 1991–2001, and may indicate a countrywide trend of increasing spillover of human tuberculosis to wild animals. South Africa ranks among the countries with the highest-tuberculosis burden worldwide, complicated by an increasing rate of multidrug-resistant strains. Exposure and infection of captive wildlife in this high prevalence setting is therefore a growing concern for wildlife conservation but also for human health through potential spillback.
... Although human populations are a demonstrated source of pathogen exchange for NHPs (Epstein & Price 2009), our data imply that habitat disturbance and anthropogenic contact may differently affect the dynamics of parasite infection and disease transmission for different NHP species. Specifically, the ability of vervets and several other Old World primates (e.g. ...
Article
Full-text available
A growing focus of nonhuman primate conservation and management planning concerns factors affecting the dynamics of parasite infection and disease transmission. Here, we examine the effects of anthropogenic and environmental components of the landscape on the prevalence, richness, and species diversity of gastrointestinal parasites in wild-caught vervet monkeys (Chlorocebus aethiops) in South Africa. Nematodes of the genus Trichuris and the family Strongylidae and protists of the subclass Coccidia were present in 55.13% of the sampled animals (n=43). Parasitological, geographic and climatic correlates of infection were assessed in a geographical information systems (GIS) platform. The findings of this study suggest that parasitism in South Africa vervets may be better predicted by environmental factors than by degree of anthropogenic contact. This research represents one of the first surveys of parasitic infection in a wild money species in southern Africa.
... All things considered, this kind of investigation highlights the importance of coproparasitological surveys as part of practice in zoos in order to implement preventive measures and safeguard the health of captive animals and people near them (animal keepers and visitors). In this context, it is appropriate to take into account that the transmission of pathogens between humans and nonhuman species has to be considered in either direction, so that recognizing the links between human, animal and ecosystem health can provide an effective approach to understanding the transmission of pathogens among these hosts8. ...
Article
Full-text available
Giardia infections in captive nonhuman primates (NHP) housed at a Brazilian zoo were investigated in order to address their zoonotic potential. Fresh fecal samples were collected from the floors of 22 enclosures where 47 primates of 18 different species were housed. The diagnosis of intestinal parasites after concentration by sedimentation and flotation methods revealed the following parasites and their frequencies: Giardia (18%); Entamoeba spp. (18%); Endolimax nana (4.5%); Iodamoeba spp. (4.5%); Oxyurid (4.5%) and Strongylid (4.5%). Genomic DNA extracted from all samples was processed by PCR methods in order to amplify fragments of gdh and tpi genes of Giardia. Amplicons were obtained from samples of Ateles belzebuth, Alouatta caraya, Alouatta fusca and Alouatta seniculus. Clear sequences were only obtained for the isolates from Ateles belzebuth (BA1), Alouatta fusca (BA2) and Alouatta caraya (BA3). According to the phenetic analyses of these sequences, all were classified as assemblage A. For the tpi gene, all three isolates were grouped into sub-assemblage AII (BA1, BA2 and BA3) whereas for the gdh gene, only BA3 was sub-assemblage AII, and the BA1 and BA2 were sub-assemblage AI. Considering the zoonotic potential of the assemblage A, and that the animals of the present study show no clinical signs of infection, the data obtained here stresses that regular coproparasitological surveys are necessary to implement preventive measures and safeguard the health of the captive animals, of their caretakers and of people visiting the zoological gardens.
... However, less commonly discussed are instances of anthropozoonoses, where the so-called human diseases are transmitted to wild animals, either in captivity or when living in proximity to human communities that may have encroached upon previously pristine habitats. As expanding human populations come into ever-closer contact with wild animals, and as conservation measures increasingly involve maintenance of wildlife populations ex situ, the potential for disease transmission from humans requires careful monitoring (Epstein and Price 2009). ...
Article
Ngamba Island Chimpanzee Sanctuary (NICS) in Lake Victoria, Uganda is currently home to 44 wild-borne, semi-captive chimpanzees. Despite regular veterinary health checks, it only came to light recently that many animals, and sanctuary staff, were naturally infected with Schistosoma mansoni. Indeed, local schistosome transmission appears firmly engrained for intermediate snail hosts can be found along almost the entirety of Ngamba's shoreline. Here, the epidemiology of infection is a dynamic interplay between human and chimpanzee populations, as revealed by genetic analyses of S. mansoni. In this review, our present understanding of this complex and evolving situation is discussed, alongside general disease control activities in Uganda, to highlight future interventions towards stopping schistosome morbidity and transmission within this conservation sanctuary setting.
Article
Market integration (MI), or the shift from subsistence to market-based livelihoods, profoundly influences health, yet its impacts on infectious diseases remain underexplored. Here, we synthesize the current understanding of MI and infectious disease to stimulate more research, specifically aiming to leverage concepts and tools from disease ecology and related fields to generate testable hypotheses. Embracing a One Health perspective, we examine both human-to-human and zoonotic transmission pathways in their environmental contexts to assess how MI alters infectious disease exposure and susceptibility in beneficial, detrimental and mixed ways. For human-to-human transmission, we consider how markets expand contact networks in ways that facilitate infectious disease transmission while also increasing access to hygiene products and housing materials that likely reduce infections. For zoonotic transmission, MI influences exposures to pathogens through agricultural intensification and other market-driven processes that may increase or decrease human encounters with disease reservoirs or vectors in their shared environments. We also consider how MI-driven changes in noncommunicable diseases affect immunocompetence and susceptibility to infectious disease. Throughout, we identify statistical, survey and laboratory methods from ecology and the social sciences that will advance interdisciplinary research on MI and infectious disease.
Article
Retroviruses replicate by means of reverse transcription, utilizing an enzyme, reverse transcriptase, in conjunction with integrase. Their elements have been found in humans, animals, fungi, plants, and bacteria alike. For millions of years, these elements are continuing to integrate into the eukaryotic genomes and affecting these organisms to date. Specifically, endogenous retroviruses have been shown to comprise a large portion of vertebrate genomes. Studies have shown that these microscopic viral elements within the genome are influencing gene expression and in turn evolution, by affecting adjacent gene expression patterns. In the medical field, these retroviruses can present illnesses for many, such as those living with Human Immunodeficiency Virus or Human T Cell Lymphotropic Viruses. With modern advances in bioinformatics, genomics, and drug design, retroviruses are being understood much better. A multitude of new discoveries is advancing the scientific communities to mitigate, prevent, and hopefully cure serious medical ailments caused by retroviruses.
Article
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Some animal species have been presumed to be purely diurnal. Yet, they show flexibility in their activity rhythm, and can occasionally be active at night. Recently, it has been suggested that chimpanzees may rarely engage in nocturnal activities in savannah forests, in contrast to the frequent nocturnal feeding of crops observed at Sebitoli, Kibale National Park, Uganda. Here we thus aimed to explore the factors that might trigger such intense nocturnal activity (e.g. harsher weather conditions during daytime, low wild food availability or higher diurnal foraging risk) in this area. We used camera-traps set over 18 km² operating for 15 months. We report activities and group composition from records obtained either within the forest or at the forest interface with maize fields, the unique crop consumed. Maize is an attractive and accessible food source, although actively guarded by farmers, particularly during daytime. Out of the 19 156 clips collected, 1808 recorded chimpanzees. Of these, night recordings accounted for 3.3% of forest location clips, compared to 41.8% in the maize fields. Most nocturnal clips were obtained after hot days, and most often during maize season for field clips. At night within the forest, chimpanzees were travelling around twilight hours, while when at the border of the fields they were foraging on crops mostly after twilight and in smaller parties. These results suggest that chimpanzees change their activity rhythm to access cultivated resources when human presence and surveillance is lower. This survey provides evidence of behavioral plasticity in chimpanzees in response to neighboring human farming activities, and emphasizes the urgent need to work with local communities to mitigate human-wildlife conflict related to crop-feeding.
Chapter
The majority of all emerging pathogens in humans are zoonotic (nonhuman animal) in origin. Population, ecological, and behavioral changes that increase contact with wildlife exacerbate emergence of these pathogens. Anthropogenic modification of the physical environment has altered not only our risk of zoonotic infection from wildlife but also the likelihood of pathogen transmission from human to nonhuman animal populations. This is particularly the case for primates that share a number of common infections with humans. In this chapter, I use a series of case studies involving SARS, HIV, Nipah virus, Lyme disease, malaria, and Ebola to exemplify how various anthropogenic factors have facilitated pathogen transmission between human and nonhuman animal populations. The costs and benefits of primate-based ecotourism are also reviewed to better illustrate how human-wildlife contact can affect both populations. Responsible health monitoring of human-wildlife interactions is a necessary prerequisite for prevention of the transmission of future emerging infectious diseases.
Chapter
Epizootiology is an area of epidemiological science which entails the study and control of disease in animals. This term is synonymous with the more popular idiom veterinary epidemiology. Epizootiologic activities include herd or population health surveillance, outbreak investigation, clinical trials, diagnostic test validation, mathematical disease modeling, and risk assessment to support the control and prevention of disease in animal populations.
Chapter
The majority of emerging zoonoses, including those for which bats are a natural reservoir, such as Ebolaviruses, SARS coronaviruses, Nipah virus and Hendra virus, are driven by human activities. These activities include deforestation, agricultural intensification, bushmeat hunting, and wildlife trade, and, fundamentally, escalate contact between human and wildlife populations. In order to mitigate emergence, outbreaks and potential pandemics, it is imperative that we understand the ecology of these viruses and their hosts. Little is known about the epidemiology of zoonotic viruses, though recent research has shed some light on the mechanisms by which viral spillover from bats occurs. Conducting epidemiological studies of high-risk zoonotic viruses in bats is challenging, and comprehensive multidisciplinary studies employing an ecosystem health (“One Health”) approach are necessary to develop simple and effective strategies to reduce contact between humans, livestock, and bats, and reduce the risk of spillover. Such studies span host ecology, viral genetics, epidemiology, and human behavior. The continued expansion of human populations will further threaten ecosystem stability, and simple and effective behavioral changes are needed to mitigate the risk of potentially catastrophic future disease emergence. In this chapter we review investigations of the emergence of recent bat-borne zoonotic viruses and discuss underlying anthropogenic drivers.
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By integrating this study in a stess-ecology Framework, the aim of this thesis is to assess exposure and effects of trace metals (TMs) and parasitism on wood mouse[…] and to contribute to the development of non-lethal exposure and toxicity makers […].This study also reveals that the accumulations of the TMs in wood mice is influenced by individual characteristics […] and landscape features and varies according to the trapping session. In addition, results show that the concentrations of TMs […] and landscape characteristics modulate the prevalence of some parasites. […].However, given the potential effects of parasitism on animals’ health, the causal links between the presence of TMs and observed alterations are questionable. This work emphasizes the importance of multi-stress approaches on wildlife’s health assessment.
Chapter
Tuberculosis is a disease of humans and animals that is caused by the Mycobacterium tuberculosis complex (MTC). Tuberculosis is typically spread through the airborne route via droplet nuclei that are inhaled into the lungs. The majority of exposed hosts do not become infected, and the majority of infected hosts do not progress to clinically evident tuberculosis disease. However, when active tuberculosis disease does occur, it results in severe illness that is often highly contagious, commonly results in permanent damage to the lungs and other tissues, and frequently is eventually fatal without appropriate treatment. Although intraspecies (i.e., human-to-human and animal-to-animal) transmission is most common in tuberculosis epidemiology, interspecies (e.g., animal-to-human or human-to-animal) transmission is an important source of tuberculosis infections, particularly in developing areas of the world without fully developed bovine tuberculosis eradication programs and widespread pasteurization of milk. Zoonotic tuberculosis caused by Mycobacterium bovis is more common than zoonotic tuberculosis caused by other species of MTC, and tuberculosis disease caused by M. bovis infections often involve the alimentary tract, reflecting the role of ingestion in the transmission of M. bovis. Although rare, M. tuberculosis does play a role in transmission of tuberculosis to humans from animals such as nonhuman primates and elephants. As M. tuberculosis is host adapted to humans, infections with this MTC species in animals are generally considered to be the result of transmission from humans to animals. Prevention and control of both intraspecies and zoonotic transmission of MTC is important to eventually eliminating tuberculosis in human and domestic animal populations.
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Research regarding zoonotic diseases often focuses on infectious diseases animals have given to humans. However, an increasing number of reports indicate that humans are transmitting pathogens to animals. Recent examples include methicillin-resistant Staphylococcus aureus, influenza A virus, Cryptosporidium parvum, and Ascaris lumbricoides. The aim of this review was to provide an overview of published literature regarding reverse zoonoses and highlight the need for future work in this area. An initial broad literature review yielded 4763 titles, of which 4704 were excluded as not meeting inclusion criteria. After careful screening, 56 articles (from 56 countries over three decades) with documented human-to-animal disease transmission were included in this report. In these publications, 21 (38%) pathogens studied were bacterial, 16 (29%) were viral, 12 (21%) were parasitic, and 7 (13%) were fungal, other, or involved multiple pathogens. Effected animals included wildlife (n = 28, 50%), livestock (n = 24, 43%), companion animals (n = 13, 23%), and various other animals or animals not explicitly mentioned (n = 2, 4%). Published reports of reverse zoonoses transmission occurred in every continent except Antarctica therefore indicating a worldwide disease threat. As we see a global increase in industrial animal production, the rapid movement of humans and animals, and the habitats of humans and wild animals intertwining with great complexity, the future promises more opportunities for humans to cause reverse zoonoses. Scientific research must be conducted in this area to provide a richer understanding of emerging and reemerging disease threats. As a result, multidisciplinary approaches such as One Health will be needed to mitigate these problems.
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The majority of all emerging pathogens in humans are zoonotic (nonhu-man animal) in origin. Population, ecological, and behavioral changes that increase contact with wildlife exacerbate emergence of these pathogens. Anthropogenic modification of the physical environment has altered not only our risk of zoonotic infection from wildlife but also the likelihood of pathogen transmission from human to nonhuman animal populations. This is particularly the case for primates that share a number of common infections with humans. In this chapter, I use a series of case studies involving SARS, HIV, Nipah virus, Lyme disease, malaria, and Ebola to exemplify how various anthropogenic factors have facilitated pathogen transmission between human and nonhuman animal populations. The costs and benefits of primate-based ecotourism are also reviewed to better illustrate how human-wildlife contact can affect both populations. Responsible health monitoring of human-wildlife interactions is a necessary prerequisite for prevention of the transmission of future emerging infectious diseases.
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Understanding the emergence of new zoonotic agents requires knowledge of pathogen biodiversity in wildlife, human-wildlife interactions, anthropogenic pressures on wildlife populations, and changes in society and human behavior. We discuss an interdisciplinary approach combining virology, wildlife biology, disease ecology, and anthropology that enables better understanding of how deforestation and associated hunting leads to the emergence of novel zoonotic pathogens.
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Background: On April 15 and April 17, 2009, novel swine-origin influenza A (H1N1) virus (S-OIV) was identified in specimens obtained from two epidemiologically unlinked patients in the United States. The same strain of the virus was identified in Mexico, Canada, and elsewhere. We describe 642 confirmed cases of human S-OIV infection identified from the rapidly evolving U.S. outbreak. Methods: Enhanced surveillance was implemented in the United States for human infection with influenza A viruses that could not be subtyped. Specimens were sent to the Centers for Disease Control and Prevention for real-time reverse-transcriptase-polymerase-chain-reaction confirmatory testing for S-OIV. Results: From April 15 through May 5, a total of 642 confirmed cases of S-OIV infection were identified in 41 states. The ages of patients ranged from 3 months to 81 years; 60% of patients were 18 years of age or younger. Of patients with available data, 18% had recently traveled to Mexico, and 16% were identified from school outbreaks of S-OIV infection. The most common presenting symptoms were fever (94% of patients), cough (92%), and sore throat (66%); 25% of patients had diarrhea, and 25% had vomiting. Of the 399 patients for whom hospitalization status was known, 36 (9%) required hospitalization. Of 22 hospitalized patients with available data, 12 had characteristics that conferred an increased risk of severe seasonal influenza, 11 had pneumonia, 8 required admission to an intensive care unit, 4 had respiratory failure, and 2 died. The S-OIV was determined to have a unique genome composition that had not been identified previously. Conclusions: A novel swine-origin influenza A virus was identified as the cause of outbreaks of febrile respiratory infection ranging from self-limited to severe illness. It is likely that the number of confirmed cases underestimates the number of cases that have occurred.
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All six great apes, gorillas Gorilla gorilla and G. beringei, chimpanzees Pan troglodytes and P. paniscus, and orang-utans Pongo pygmaeus and P. abelii, are categorized as Endangered on the 2000 IUCN Red List and face many threats to their continued existence in the wild. These threats include loss of habitat to settlement, logging and agriculture, illegal hunting for bushmeat and traditional medicine, the live ape trade, civil unrest and infectious diseases. The great apes are highly susceptible to many human diseases, some of which can be fatal while others can cause marked morbidity. There is increasing evidence that diseases can be transmitted from humans to free-living habituated apes, sometimes with serious consequences. If protective measures are not improved, ape populations that are frequently in close contact with people will eventually be affected by the inadvertent transmission of human diseases. This paper describes the risks, sources and circumstances of infectious disease transmission from humans to great apes during and consequent upon habituation for tourism and research. A major problem is that the regulations that protect habituated apes from the transmission of disease from people are often poorly enforced. Suggestions are made for improving the enforcement of existing regulations governing ape-based tourism, and for minimizing the risk of disease transmission between humans, both local people and international visitors, and the great apes.
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In this review we examine the hypothesis that aquatic birds are the primordial source of all influenza viruses in other species and study the ecological features that permit the perpetuation of influenza viruses in aquatic avian species. Phylogenetic analysis of the nucleotide sequence of influenza A virus RNA segments coding for the spike proteins (HA, NA, and M2) and the internal proteins (PB2, PB1, PA, NP, M, and NS) from a wide range of hosts, geographical regions, and influenza A virus subtypes support the following conclusions. (i) Two partly overlapping reservoirs of influenza A viruses exist in migrating waterfowl and shorebirds throughout the world. These species harbor influenza viruses of all the known HA and NA subtypes. (ii) Influenza viruses have evolved into a number of host-specific lineages that are exemplified by the NP gene and include equine Prague/56, recent equine strains, classical swine and human strains, H13 gull strains, and all other avian strains. Other genes show similar patterns, but with extensive evidence of genetic reassortment. Geographical as well as host-specific lineages are evident. (iii) All of the influenza A viruses of mammalian sources originated from the avian gene pool, and it is possible that influenza B viruses also arose from the same source. (iv) The different virus lineages are predominantly host specific, but there are periodic exchanges of influenza virus genes or whole viruses between species, giving rise to pandemics of disease in humans, lower animals, and birds. (v) The influenza viruses currently circulating in humans and pigs in North America originated by transmission of all genes from the avian reservoir prior to the 1918 Spanish influenza pandemic; some of the genes have subsequently been replaced by others from the influenza gene pool in birds. (vi) The influenza virus gene pool in aquatic birds of the world is probably perpetuated by low-level transmission within that species throughout the year. (vii) There is evidence that most new human pandemic strains and variants have originated in southern China. (viii) There is speculation that pigs may serve as the intermediate host in genetic exchange between influenza viruses in avian and humans, but experimental evidence is lacking. (ix) Once the ecological properties of influenza viruses are understood, it may be possible to interdict the introduction of new influenza viruses into humans.
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Sera from a very high proportion of the human adults and new-born infants studied neutralized swine influenza virus; sera from children below the age of 12 years seldom exerted such an effect. The results of neutralization experiments with human sera and the virus of swine influenza have been compared with the outcome of similar tests with the virus of human influenza, and it seems evident that the presence of antibodies neutralizing swine influenza virus cannot be deemed the result of repeated exposures to the current human type of virus. From the known history of swine influenza and the similarity of its etiologic virus to that obtained from man it seems likely that the virus of swine influenza is the surviving prototype of the agent primarily responsible for the great human pandemic of 1918, as Laidlaw has already suggested. The presence in human sera of antibodies neutralizing swine influenza virus is believed to indicate a previous immunizing exposure to, or infection with, an influenza virus of the 1918 type.
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To determine whether dogs that visited human health-care facilities were at greater risk of acquiring certain health-care-associated pathogens, compared with dogs performing animal-assisted interventions in other settings, and to identify specific behaviors of dogs associated with an increased risk of acquiring these pathogens. Prospective cohort and nested case-control studies. 96 dogs that visited human health-care facilities and 98 dogs involved in other animal-assisted interventions. Fecal samples and nasal swab specimens were collected from dogs at the time of recruitment and every 2 months for 1 year and were tested for methicillin-resistant Staphylococcus aureus (MRSA), Clostridium difficile, and other selected bacteria. Information was also obtained on facilities visited during animal-assisted interventions, dog diet, dog illnesses, and antimicrobial use within the home. At the end of the study, dog handlers were asked about the behavior of their dogs during visits to health-care facilities. Rates of acquisition of MRSA and C difficile were 4.7 and 2.4 times as high, respectively, among dogs that visited human health-care facilities, compared with rates among dogs involved in other animal-assisted interventions. Among dogs that visited human health-care facilities, those that licked patients or accepted treats during visits were more likely to be positive for MRSA and C difficile than were dogs that did not lick patients or accept treats. Results suggested that dogs that visited human health-care facilities were at risk of acquiring MRSA and C difficile, particularly when they licked patients or accepted treats during visits.
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Methicillin-resistant Staphylococcus aureus (MRSA) is increasing worldwide. Occasionally, animals are colonized or infected incidentally with human strains. Recently, however, new strains of MRSA emerging from within the animal kingdom, particularly in pigs, are causing human infection. MRSA has been reported in species as diverse as companion animals, horses and pigs, through to chinchillas, bats and parrots. In contrast, whereas strains of community-associated MRSA, the majority of which carry genes encoding Panton-Valentine leucocidin, are spreading rapidly in human populations, only sporadic cases have been reported in animals to date. Although MRSA has been found in some meat products, the implications for human infection through consumption are unclear. This review examines the epidemiology of MRSA in animals and human attendants/owners, the diagnosis and management of MRSA colonization, infection and infection control strategies in animals.
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We conducted a prospective study of bacterial transmission among humans, nonhuman primates (primates hereafter), and livestock in western Uganda. Humans living near forest fragments harbored Escherichia coli bacteria that were approximately 75% more similar to bacteria from primates in those fragments than to bacteria from primates in nearby undisturbed forests. Genetic similarity between human/livestock and primate bacteria increased approximately 3-fold as anthropogenic disturbance within forest fragments increased from moderate to high. Bacteria harbored by humans and livestock were approximately twice as similar to those of red-tailed guenons, which habitually enter human settlements to raid crops, than to bacteria of other primate species. Tending livestock, experiencing gastrointestinal symptoms, and residing near a disturbed forest fragment increased genetic similarity between a participant's bacteria and those of nearby primates. Forest fragmentation, anthropogenic disturbance within fragments, primate ecology, and human behavior all influence bidirectional, interspecific bacterial transmission. Targeted interventions on any of these levels should reduce disease transmission and emergence.
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Between 1994 and 1996, three elephants from an exotic animal farm in Illinois died of pulmonary disease due to Mycobacterium tuberculosis. In October 1996, a fourth living elephant was culture-positive for M. tuberculosis. Twenty-two handlers at the farm were screened for tuberculosis (TB); eleven had positive reactions to intradermal injection with purified protein derivative. One had smear-negative, culture-positive active TB. DNA fingerprint comparison by IS6110 and TBN12 typing showed that the isolates from the four elephants and the handler with active TB were the same strain. This investigation indicates transmission of M. tuberculosis between humans and elephants.
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A case of zoonotic Mycobacterium tuberculosis infection in a marmoset (Callithrix jacchus) is reported. Genomic typing of the relevant M. tuberculosis isolates strongly suggests that the marmoset, which was kept as companion animal, acquired the disease from an infected member in the household who had been treated for pulmonary tuberculosis 8 years prior to this case.
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A measles outbreak in a facility housing Old World nonhuman primates developed over a 2-month period in 1996, providing an opportunity to study the epidemiology of this highly infectious disease in an animal-handling setting. Serum and urine specimens were collected from monkeys housed in the room where the initial measles cases were identified, other monkeys with suspicious measles-like signs, and employees working in the affected areas. Serum specimens were tested for measles virus-specific IgG and IgM antibodies, and urine specimens were tested for measles virus by virus isolation or reverse transcriptase-polymerase chain reaction (RT-PCR). A total of 94 monkeys in two separate facilities had evidence of an acute measles infection. The outbreak was caused by a wild-type virus that had been associated with recent human cases of acute measles in the United States; however, an investigation was unable to identify the original source of the outbreak. Quarantine and massive vaccination helped to control further spread of infection. Results emphasize the value of having a measles control plan in place that includes a preventive measles vaccination program involving human and nonhuman primates to decrease the likelihood of a facility outbreak.
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Emerging infectious diseases (EIDs) of free-living wild animals can be classified into three major groups on the basis of key epizootiological criteria: (i) EIDs associated with “spill-over” from domestic animals to wildlife populations living in proximity; (ii) EIDs related directly to human intervention, via host or parasite translocations; and (iii) EIDs with no overt human or domestic animal involvement. These phenomena have two major biological implications: first, many wildlife species are reservoirs of pathogens that threaten domestic animal and human health; second, wildlife EIDs pose a substantial threat to the conservation of global biodiversity.
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From 1997 to 2000, Mycobacterium tuberculosis was diagnosed in two Asian elephants (Elephas maximus), three Rocky Mountain goats (Oreamnos americanus), and one black rhinoceros (Diceros bicornis) in the Los Angeles Zoo. DNA fingerprint patterns suggested recent transmission. An investigation found no active cases of tuberculosis in humans; however, tuberculin skin-test conversions in humans were associated with training elephants and attending an elephant necropsy.
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Emerging Human Infectious Diseases: Anthroponoses, Zoonoses, and Sapronoses To the Editor: The source of infection has always been regarded as an utmost factor in epidemiology. Human communicable diseases can be classified according to the source of infection as anthroponoses (when the source is an infectious human; interhuman transfer is typical), zoonoses (the source is an infectious animal; interhuman transfer is uncommon), and sapronoses (the source is an abiotic substrate, nonliving environment; interhuman transfer is exceptional). The source of infection is often the reservoir or, in ecologic terms, the habitat where the etiologic agent of the disease normally thrives, grows, and replicates. A characteristic feature of most zoonoses and sapronoses is that once transmitted to humans, the epidemic chain is usually aborted, but the clinical course might be sometimes quite severe, even fatal. An ecologic rule specifies that an obligatory parasite should not kill its host to benefit from the adapted long-term symbiosis, whereas an occasionally attacked alien host, such as a human, might be subjected to a severe disease or even killed rapidly by the parasite because no evolutionary adaptation to that host exists (1). In this letter, only microbial infections are discussed; metazoan invasion and infestations have been omitted. Anthroponoses (Greek “anthrópos” = man, “nosos” = disease) are diseases transmissible from human to human. Examples include rubella, smallpox, diphtheria, gonorrhea, ringworm (Trichophyton rubrum), and trichomoniasis. Zoonoses (Greek “zoon” = animal) are diseases transmissible from living animals to humans (2). These diseases were formerly called anthropozoonoses, and the diseases transmissible from humans to animals were called zooanthroponoses. Unfortunately, many scientists used these terms in the reverse sense or indiscriminately, and an expert committee decided to abandon these two terms and recommended “zoonoses” as “diseases and infections which are naturally transmitted between vertebrate animals and man” (3). A limited number of zoonotic agents can cause extensive outbreaks; many zoonoses, however, attract the public’s attention because of the high death rate associated with the infections. In addition, zoonoses are sometimes contagious for hospital personnel (e.g., hemorrhagic fevers). Zoonotic diseases can be classified according to the ecosystem in which they circulate. The classification is either synanthropic zoonoses, with an urban (domestic) cycle in which the source of infection are domestic and synanthropic animals (e.g., urban rabies, cat scratch disease, and zoonotic ringworm) or exoanthropic zoonoses, with a sylvatic (feral and wild) cycle in natural foci (4) outside human habitats (e.g., arboviroses, wildlife rabies, Lyme disease, and tularemia). However, some zoonoses can circulate in both urban and natural cycles (e.g., yellow fever and Chagas disease). A number of zoonotic agents are arthropod-borne (5); others are transmitted by direct contact, alimentary (foodborne and waterborne), or aerogenic (airborne) routes; and some are rodent-borne. Sapronoses (Greek “sapros” = decaying; “sapron” means in ecology a decaying organic substrate) are human diseases transmissible from abiotic environment (soil, water, decaying plants, or animal corpses, excreta, and other substrata). The ability of the agent to grow saprophytically and replicate in these substrata (i.e., not only to survive or contaminate them secondarily) are the most important characteristics of a sapronotic microbe. Sapronotic agents thus carry on two diverse ways of life: saprophytic (in an abiotic substrate at ambient temperature) and parasitic (pathogenic, at the temperature of a homeotherm vertebrate host). Typical sapronoses are visceral mycoses caused by dimorphic fungi (e.g., coccidioidomycosis and histoplasmosis), “monomorphic” fungi (e.g., aspergillosis and cryptococcosis), certain superficial mycoses (Microsporum gypseum), some bacterial diseases (e.g., legionellosis), and protozoan (e.g., primary amebic meningoencephalitis). Intracellular parasites of animals (viruses, rickettsiae, and chlamydiae) cannot be sapronotic agents. The term “sapronosis” was introduced in epidemiology as a useful concept (6–8). For these diseases the expert committee applied the term “sapro-zoonoses,” defined as “having both a vertebrate host and a nonanimal developmental site or reservoir (organic matter, soil, and plants)” (3,9). However, the term sapronoses is more appropriate because animals are not the source of infection for humans. While anthroponoses and zoonoses are usually the domains for professional activities of human and veterinary microbiologists, respectively, sapronoses may be the domain for environmental microbiologists. The underdiagnosis rate for sapronoses is probably higher than that for anthroponoses and zoonoses, and an increase should be expected in both incidence and number of sapronoses. Legionellosis, Pontiac fever, nontuberculous mycobacterioses, and primary amebic meningoencephalitis are a few sapronoses that have emerged in the past decade. In addition, the number of opportunistic infections in immunosuppressed patients has grown markedly; many of these diseases and some nosocomial infections are, in fact, also sapronoses. As with any classification, grouping human diseases in epidemiologic categories according to the source of infection has certain pitfalls. Some arthropodborne diseases (urban yellow fever, dengue, epidemic typhus, tickborne relapsing fever, epidemic relapsing fever, and malaria) might be regarded as anthroponoses rather than zoonoses because the donor of the infectious blood for the vector is an infected human and not a vertebrate animal. However, the human infection is caused by an (invertebrate) animal in which the agent replicates, and the term zoonoses is preferred. HIV is of simian origin with a sylvatic cycling among wild primates and accidental infection of humans who hunted or ate them; the human disease (AIDS) might thus have been regarded as a zoonosis in the very first phase but later has spread in the human population as a typical anthroponosis and caused the present pandemic. Similarly, pandemic strains of influenza developed through an antigenic shift from avian influenza A viruses. For some etiologic agents or their genotypes, both animals and humans are concurrent reservoirs (hepatitis virus E, Norwalk-like calicivirus, enteropathogenic Escherichia coli, Pneumocystis, Cryptosporidium, Giardia, and Cyclospora); these diseases might conditionally be called anthropozoonoses. Other difficulties can occur with classifying diseases caused by sporulating bacteria (Clostridium and Bacillus): Their infective spores survive in the soil or in other substrata for very long periods, though they are usually produced after a vegetative growth in the abiotic environment, which can include animal carcasses. These diseases should therefore be called sapronoses. For some other etiologic agents, both animals and abiotic environment can be the reservoir (Listeria, Erysipelothrix, Yersinia pseudotuberculosis, Burkholderia pseudomallei, and Rhodococcus equi), and the diseases might be, in fact, called saprozoonosis (not sensu 9 ) in that their source can be either an animal or an abiotic substrate. For a concise list of anthropo-, zoo-, and sapronoses, see the online appendix (available from: URL: http://www. cdc.gov/ncidod/EID/vol9no3/02-0208- app.htm. Zdenek Hubálek* *Academy of Sciences, Brno, Czech Republic References 1. Lederberg J. Infectious disease as an evolutionary paradigm. Emerg Infect Dis 1997;3:417–23. 2. Bell JC, Palmer SR, Payne JM. The zoonoses (infections transmitted from animals to man). London: Arnold; 1988. 3.World Health Organization. Joint WHO/FAO expert committee on zoonoses. 2nd report. WHO technical report series no. 169, Geneva; 1959. 3rd report, WHO Technical Report Series no. 378, Geneva; The Organization; 1967. 4. Pavlovsky EN. Natural nidality of transmissible diseases. Urbana (IL): University of Illinois Press; 1966. 5. Beaty BJ, Marquardt WC, editors. The biology of disease vectors. Niwot (CO): University Press of Colorado; 1996. 6. Terskikh VI. Diseases of humans and animals caused by microbes able to reproduce in an abiotic environment that represents their living habitat (in Russian). Zhurn Mikrobiol Epidemiol Immunobiol (Moscow) 1958;8:118–22. 7. Somov GP, Litvin VJ. Saprophytism and parasitism of pathogenic bacteria—ecological aspects (in Russian). Novosibirsk: Nauka; 1988. 8. Krauss H, Weber A, Enders B, Schiefer HG, Slenczka W, Zahner H. Zoonosen, 2. Aufl. Köln: Deutscher Ärzte-Verlag; 1997. 9. Schwabe CV. Veterinary medicine and human health. Baltimore: Williams & Wilkins; 1964. Address for correspondence: Zdenek Hubálek, Institute of Vertebrate Biology, Academy of Sciences, Klásterní 2, CZ-69142 Valtice, Czech Republic; fax: 420-519352387; e-mail: zhubalek@ brno.cas.cz Multidrug-
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In this review we examine the hypothesis that aquatic birds are the primordial source of all influenza viruses in other species and study the ecological features that permit the perpetuation of influenza viruses in aquatic avian species. Phylogenetic analysis of the nucleotide sequence of influenza A virus RNA segments coding for the spike proteins (HA, NA, and M2) and the internal proteins (PB2, PB1, PA, NP, M, and NS) from a wide range of hosts, geographical regions, and influenza A virus subtypes support the following conclusions. (i) Two partly overlapping reservoirs of influenza A viruses exist in migrating waterfowl and shorebirds throughout the world. These species harbor influenza viruses of all the known HA and NA subtypes. (ii) Influenza viruses have evolved into a number of host-specific lineages that are exemplified by the NP gene and include equine Prague/56, recent equine strains, classical swine and human strains, H13 gull strains, and all other avian strains. Other genes show similar patterns, but with extensive evidence of genetic reassortment. Geographical as well as host-specific lineages are evident. (iii) All of the influenza A viruses of mammalian sources originated from the avian gene pool, and it is possible that influenza B viruses also arose from the same source. (iv) The different virus lineages are predominantly host specific, but there are periodic exchanges of influenza virus genes or whole viruses between species, giving rise to pandemics of disease in humans, lower animals, and birds. (v) The influenza viruses currently circulating in humans and pigs in North America originated by transmission of all genes from the avian reservoir prior to the 1918 Spanish influenza pandemic; some of the genes have subsequently been replaced by others from the influenza gene pool in birds. (vi) The influenza virus gene pool in aquatic birds of the world is probably perpetuated by low-level transmission within that species throughout the year. (vii) There is evidence that most new human pandemic strains and variants have originated in southern China. (viii) There is speculation that pigs may serve as the intermediate host in genetic exchange between influenza viruses in avian and humans, but experimental evidence is lacking. (ix) Once the ecological properties of influenza viruses are understood, it may be possible to interdict the introduction of new influenza viruses into humans.
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An outbreak of natural measles virus infection occurred in a group of Japanese macaques (Macaca fuscata). Over a period of 4 months, 12 of 53 Japanese macaques died following a 2-23-day history of anorexia, diarrhea, and dermatitis. The monkeys were kept in outdoor exhibits but had been moved temporarily into indoor caging and then transferred to new outdoor exhibits. Ten monkeys died while they were in temporary caging, and two monkeys died after they were moved to new outdoor exhibits. The diagnoses were made based on the results of histopathology, immunohistochemistry (IHC), in situ hybridization (ISH), and electron microscopy. Measles virus antigens were detected in the lung, stomach, skin, salivary gland, spleen, and lymph nodes. Tangled, tubular nucleocapsids compatible with paramyxovirus were noted in the lung tissue. As a result of immunosuppression following measles virus infection, various secondary infections including disseminated cytomegalovirus infection, adenoviral and bacterial pneumonia, and Candida albicans-associated gingivitis and esophagitis were noted. The primary infective source or the mode of infection could not be determined in this outbreak, but measles virus may have been transmitted to the monkeys from human visitors while the monkeys were on exhibit.
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Ecological overlap may increase the risks of microbial exchange between humans and wild non-human primates. Escherichia coli bacteria were collected from chimpanzees and humans in Kibale National Park, western Uganda, in May and June 2004, in order to examine whether interaction between humans and apes in the wild might affect gastrointestinal bacterial communities in the two species. Chimpanzees harbored bacteria genetically more similar to those of humans employed in chimpanzee-directed research and tourism than to those of humans from a local village. Most humans (81.6%) and 4.4% of chimpanzees harbored at least one isolate resistant to locally available antibiotics. In isolates from both humans and chimpanzees, resistance was higher to five of these antibiotics than to Ceftiofur, an antibiotic not available in the region. These data indicate that humans and apes interacting in the wild can share genetically and phenotypically similar gastrointestinal bacteria, presumably originating from common environmental sources. Strategies to limit transmission of pathogens between humans and primates, whether that transmission is direct or indirect, would benefit both human health and primate conservation.
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Mycobacterium tuberculosis was isolated from the eyelid, skin, tongue, and lungs of a green-winged macaw (Ara chloroptera). Two persons living in the same household were culture positive for pulmonary tuberculosis 3 to 4 years before tuberculosis was diagnosed in the bird. Although humans have not been shown to acquire tuberculosis from birds, an infected bird may be a sentinel for human infection.
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This book is an official report edited by APHA for information to the people about the right tools that the society requires to preventing disease transmission
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The symptomatology of the reaction induced in monkeys by inoculation with material containing the virus of measles is described. The symptoms and course of this reaction closely parallel those of human measles. The microscopic pathology of the lesions of the skin and buccal mucous membrane of monkeys experimentally infected with the virus of measles is also described. These lesions are essentially identical with the corresponding lesions of measles in man.
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Influenza viruses cause annual epidemics and occasional pandemics that have claimed the lives of millions. The emergence of new strains will continue to pose challenges to public health and the scientific communities. A prime example is the recent emergence of swine-origin H1N1 viruses that have transmitted to and spread among humans, resulting in outbreaks internationally. Efforts to control these outbreaks and real-time monitoring of the evolution of this virus should provide us with invaluable information to direct infectious disease control programmes and to improve understanding of the factors that determine viral pathogenicity and/or transmissibility.
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Meticillin-resistant Staphylococcus aureus (MRSA), usually known as a nosocomial pathogen, has emerged as the predominant cause of skin and soft-tissue infections in many communities. Concurrent with the emergence of community-acquired MRSA (CA-MRSA), there have been increasing numbers of reports of community-acquired necrotising pneumonia in young patients and others without the classic health-care-associated risk factors. Community-onset necrotising pneumonia due to CA-MRSA is now recognised as an emerging clinical entity with distinctive clinical features and substantial morbidity and mortality. A viral prodrome (eg, influenza or influenza-like illness) followed by acute onset of shortness of breath, sepsis, and haemoptysis is the most frequent clinical presentation. The best treatment of this partly toxin-mediated disease has not been clearly defined. Whereas cases of CA-MRSA pneumonia have now been reported from almost every continent, the overall burden of disease of this emerging syndrome remains incompletely described. We report two related cases of community-onset pneumonia due to the MRSA USA300 genotype and review the literature regarding the emergence of CA-MRSA pneumonia.
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Waterborne outbreaks of diarrhoeal illness reported worldwide are mostly associated with Cryptosporidium spp. and Giardia spp. Their presence in aquatic systems makes it essential to develop preventive strategies for water and food safety. This study was undertaken to monitor the presence of Cryptosporidium and Giardia in a total of 175 water samples, including raw and treated water from both surface and ground sources in Portugal. The samples were processed according to USEPA Method 1623 for immunomagnetic separation (IMS) of Cryptosporidium oocysts and Giardia cysts, followed by detection of oocysts/cysts by immunofluorecence (IFA) microscopy, PCR-based techniques were done on all water samples collected. Out of 175 samples, 81 (46.3%) were positive for Cryptosporidium and 67 (38.3%) for Giardia by IFA. Cryptosporidium spp. and G. duodenalis genotypes were identified by PCR in 37 (21.7%) and 9 (5.1%) water samples, respectively. C. parvum was the most common species (78.9%), followed by C. hominis (13.2%), C. andersoni (5.3%), and C. muris (2.6%). Subtype IdA15 was identified in all C. hominis-positive water samples. Subtyping revealed the presence of C. parvum subtypes IIaA15G2R1, IIaA16G2R1 and IIdA17G1. Giardia duodenalis subtype A1 was identified. The results of the present study suggest that Cryptosporidium spp. and Giardia spp. were widely distributed in source water and treated water in Portugal. Moreover, the results obtained indicate a high occurrence of human-pathogenic Cryptosporidium genotypes and subtypes in raw and treated water samples. Thus, water can be a potential vehicle in the transmission of cryptosporidiosis, and giardiasis of humans and animals in Portugal.
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B virus is a zoonotic alphaherpesvirus enzootic in Asian monkeys of the genus Macaca. At least 25 cases of human disease caused by B virus have occurred to date, leading to death in 16 instances. Advances in the technology available for the diagnosis of B virus infection and in the agents for its treatment are improving the prognosis for cases in human beings. Efforts are under way at several institutions in the United States to establish B virus-free colonies of rhesus macaques for use in biomedical research. Unfortunately, the epidemiology of B virus in group-housed macaques is poorly understood. The elucidation of factors important in the transmission of B virus between monkeys will greatly enhance efforts to eradicate this virus and may help to minimize further human exposure to the agent.