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Geographic location and serologic test results for dengue virus and Leptospira spp. in nonhuman primates from Puerto Rico.
Source publication
Serum specimens from free-ranging but nonnative patas monkeys (Erythrocebus patas) and rhesus macaques (Macaca mulatta) in southwestern Puerto Rico (PR) were tested for antibodies to infection with dengue viruses (DENVs), West Nile virus (WNV), Leptospira species, and Burkholderia pseudomallei by microneutralization, plaque reduction neutralization...
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Citations
... Unlike for humans, there are few published data about disease burden in NHP, even though natural infections occur. However, a handful of reported melioidosis cases in NHP dating back to the 1920's in Malaysia, Australia, United States of America (US), India, France, Britain, and Indonesia [12][13][14][15] suggest that the burden is sporadic. These cases consisted of disease in NHP in wild colonies, zoos, and primate research centers. ...
Background:
Melioidosis is a disease caused by the bacterium Burkholderia pseudomallei, infecting humans and non-human primates (NHP) through contaminated soil or water. World-wide there are an estimated 165,000 human melioidosis cases each year, but recordings of NHP cases are sporadic. Clinical detection of melioidosis in humans is primarily by culturing B. pseudomallei, and there are no standardized detection protocols for NHP. NHP are an important animal model for melioidosis research including clinical trials and development of biodefense countermeasures.
Methodology/principle findings:
We evaluated the diagnostic potential of the multiple antigen serological assay, BurkPx, in NHP using two sera sets: (i) 115 B. pseudomallei-challenged serum samples from 80 NHP collected each week post-exposure (n = 52) and at euthanasia (n = 47), and (ii) 126 B. pseudomallei-naïve/negative serum samples. We observed early IgM antibody responses to carbohydrate antigens followed by IgG antibody recognition to multiple B. pseudomallei protein antigens during the second week of infection. B. pseudomallei negative serum samples had low to intermediate antibody cross reactivity to the antigens in this assay. Infection time was predicted as the determining factor in the variation of antibody responses, with 77.67% of variation explained by the first component of the principal component analysis. A multiple antigen model generated a binary prediction metric ([Formula: see text]), which when applied to all data resulted in 100% specificity and 63.48% sensitivity. Removal of week 1 B. pseudomallei challenged serum samples increased the sensitivity of the model to 95%.
Conclusion/significance:
We employed a previously standardized assay for humans, the BurkPx assay, and assessed its diagnostic potential for detection of B. pseudomallei exposure in NHP. The assay is expected to be useful for surveillance in NHP colonies, in investigations of suspected accidental releases or exposures, and for identifying vaccine correlates of protection.
... and the ground-dwelling Erythrocebus patas monkeys, which are the only extant non-human primates in southern Mauritania [72]. It has also been strongly suggested that patas monkeys can be naturally infected with DENV from human hosts [73]. This hypothesis would require the "West African epidemic strain" of DENV to be introduced and maintained in the local sylvatic cycle, as postulated in South America [74]. ...
The number of sporadic and epidemic dengue fever cases have reportedly been increasing in recent years in some West African countries, such as Senegal and Mali. The first epidemic of laboratory-confirmed dengue occurred in Nouakchott, the capital city of Mauritania situated in the Saharan desert, in 2014. On-site diagnosis of dengue fever was established using a rapid diagnostic test for dengue. In parallel, the presence of Aedes aegypti mosquitoes in the city was confirmed. The initial diagnosis was confirmed by RT-PCR, which showed that all samples from the 2014 dengue epidemic in Nouakchott were dengue virus serotype 2 (DENV-2). The whole genome or envelope protein gene of these strains, together with other DENV-2 strains obtained from travelers returning from West African countries to France between 2016 and 2019 (including two Mauritanian strains in 2017 and 2018), were sequenced. Phylogenetic analysis suggested a recent emergence of an epidemic strain from the cosmopolitan genotype belonging to West African cosmopolitan lineage II, which is genetically distinct from African sylvatic genotype. The origin of this DENV-2 lineage is still unknown, but our data seem to suggest a recent and rapid dispersion of the epidemic strain throughout the region. More complete genome sequences of West African DENV-2 are required for a better understanding of the dynamics of its circulation. Arboviral surveillance and outbreak forecasting are urgently needed in West Africa.
... Simian varicella virus (SVV) was first isolated in 1966 from African green monkeys (Cercopithecus aethiops) imported from Nairobi, Kenya to the Liverpool School of Tropical Medicine in the United Kingdom (UK) (Clarkson et al. 1967). SVV infection caused severe disease that resulted in a 56% case fatality rate (CFR) in the imported animals within 48 h of the appearance of a varicella-like rash (Clarkson et al. 1967;Hemme et al. 2016). The deceased animals presented with fever, widespread vesicular rash, and multiple hemorrhagic foci throughout the lungs, liver, and spleen (Clarkson et al. 1967). ...
Simian varicella virus (SVV) was first isolated in 1966 from African green monkeys (Cercopithecus aethiops) imported from Nairobi, Kenya, to the Liverpool School of Tropical Medicine in the United Kingdom (UK) (Clarkson et al., Arch Gesamte Virusforsch 22:219-234, 1967). SVV infection caused severe disease that resulted in a 56% case fatality rate (CFR) in the imported animals within 48 h of the appearance of a varicella-like rash (Clarkson et al., Arch Gesamte Virusforsch 22:219-234, 1967; Hemme et al., Am J Trop Med Hyg 94:1095-1099, 2016). The deceased animals presented with fever, widespread vesicular rash, and multiple hemorrhagic foci throughout the lungs, liver, and spleen (Clarkson et al., Arch Gesamte Virusforsch 22:219-234, 1967). This outbreak was quickly followed by a second outbreak in 47 patas monkeys (Erythrocebus patas) imported from Chad and Nigeria by Glaxo Laboratories (London, England, UK), which quickly spread within the facility (McCarthy et al., Lancet 2:856-857, 1968).
... There were 15 studies involving a forest setting [22,[24][25][26][27][28][29][30][31][32][33][34][35][36][37], 12 of which were based solely in a forest. Of 7 studies involving the urban/rural setting [26,31,[38][39][40][41][42], only 5 were exclusively based at such. Only one study involved the coastal setting [29]. ...
Dengue is a rapidly spreading mosquito-borne flavivirus infection that is prevalent in tropical and sub-tropical regions. Humans are known to be the main reservoir host maintaining the epidemic cycles of dengue but it is unclear if dengue virus is also maintained in a similar enzootic cycle. The systematic review was conducted in accordance to Cochrane's PRISMA recommendations. A search was done on PubMed, EMBASE, Scopus and Cochrane Library. Key data on animal dengue positivity was extracted and classified according to animal type and diagnostic modes. Of the 3818 articles identified, 56 articles were used in this review. A total of 16,333 animals were tested, 1817 of which were positive for dengue virus by RT-PCR or serology. Dengue positivity was detected in bats (10.1%), non-human primates (27.3%), birds (11%), bovid (4.1%), dogs (1.6%), horses (5.1%), pigs (34.1%), rodents (3.5%), marsupials (13%) and other small animals (7.3%). While majority of dengue positivity via serology suggests potential enzootic transmission, but regular dengue virus spillback cannot be excluded. With the exception of bats, acute infection among animals is limited. Further investigation on animals is critically required to better understand their role as potential reservoir in dengue transmission.
... Also, a serological investigation conducted in Puerto Rico on free living OWMs highlighted a seropositivity of nine out of twenty two Erythrocebus patas to serovars Australis, Autumnalis, Ballum, Batavie and Icterohaemorragiae [54]. ...
... Serological reactions were also detected in this species in free living animals in Puerto Rico, with prevalence ranging from 3% to 50%. The most detected serovars were Batavie an Icterohaemorrhagiae [54,59]. ...
Non-Human Primates (NHPs) are a large group of animals living in different Countries all over the World, frequently kept in captivity in zoos or in rehabilitation and research centers. In this book chapter, data available in literature on Leptospira infection in different genera and species of NHPs are reported. Few studies described clinical infections, associated to Icterohaemorrhagiae and Ballum serogroups, occurring only in captive animals. Serological positivity varies considerably among species and geographical areas, and it is difficult to define a subset of serovars more often detected by MAT. Most studies were carried out in South America on New World Monkeys and recent information about Leptospira infection in Old World Monkeys, Apes and Prosimians are scant. The exact role of NHPs in Leptospira epidemiology is not clear yet; more surveys are needed, in particular strains isolation and characterization and/or molecular analysis on both captive and wild NHPs should be of great importance.
... Limited population and environmental analyses demonstrated a seropositivity of 6 to 25% and isolation of B. pseudomallei from a soil sample (145). Furthermore, a study of Puerto Rican wildlife described a B. pseudomallei-seropositive terrestrial monkey (148). In Central America, cases have been reported from every country except for Nicaragua and Belize (138). ...
... Limited population and environmental analyses demonstrated a seropositivity of 6 to 25% and isolation of B. pseudomallei from a soil sample (145). Furthermore, a study of Puerto Rican wildlife described a B. pseudomallei-seropositive terrestrial monkey (148). In Central America, cases have been reported from every country except for Nicaragua and Belize (138). ...
The causative agent of melioidosis, Burkholderia pseudomallei , a tier 1 select agent, is endemic in Southeast Asia and northern Australia, with increased incidence associated with high levels of rainfall. Increasing reports of this condition have occurred worldwide, with estimates of up to 165,000 cases and 89,000 deaths per year. The ecological niche of the organism has yet to be clearly defined, although the organism is associated with soil and water. The culture of appropriate clinical material remains the mainstay of laboratory diagnosis. Identification is best done by phenotypic methods, although mass spectrometric methods have been described. Serology has a limited diagnostic role. Direct molecular and antigen detection methods have limited availability and sensitivity. Clinical presentations of melioidosis range from acute bacteremic pneumonia to disseminated visceral abscesses and localized infections. Transmission is by direct inoculation, inhalation, or ingestion. Risk factors for melioidosis include male sex, diabetes mellitus, alcohol abuse, and immunosuppression. The organism is well adapted to intracellular survival, with numerous virulence mechanisms. Immunity likely requires innate and adaptive responses. The principles of management of this condition are drainage and debridement of infected material and appropriate antimicrobial therapy. Global mortality rates vary between 9% and 70%. Research into vaccine development is ongoing.
... Subsequently, between 2010 and 2012, wildcaught patas monkeys (E. patas) and rhesus macaques (Macaca mulatta) from Puerto Rico had serological evidence of prior DENV infection (Table 2) [65]. As there was no evidence for sylvatic cycling of DENVs in NHPs in the Americas, the authors suggested their results might represent 'spillback' infection, with the NHPs acquiring infections as part of urban cycles involving people on the islands. ...
Abstract Arboviruses infecting people primarily exist in urban transmission cycles involving urban mosquitoes in densely populated tropical regions. For dengue, chikungunya, Zika and yellow fever viruses, sylvatic (forest) transmission cycles also exist in some regions and involve non-human primates and forest-dwelling mosquitoes. Here we review the investigation methods and available data on sylvatic cycles involving non-human primates and dengue, chikungunya, Zika and yellow fever viruses in Africa, dengue viruses in Asia and yellow fever virus in the Americas. We also present current putative data that Mayaro, o’nyong’nyong, Oropouche, Spondweni and Lumbo viruses exist in sylvatic cycles.
... In addition to the presence of B. pseudomallei in humans and the environment in Puerto Rico, Hemme et al. found the presence of antibodies against B. pseudomallei in one of 24 non-human primates (Erythrocebus patas) that were tested [55]. This study suggested probable transmission through contact with contaminated soil and water. ...
Burkholderia pseudomallei is the causative agent of melioidosis, an endemic disease in tropical areas around the world. Cumulative human cases have demonstrated that melioidosis is prevalent and increasingly recognized in the American continent. Even though the first reports of melioidosis in Mexico, Central America, and the Caribbean Islands date back to the late 1940s, the potential of the disease as a public health concern in the region has not been fully appreciated. Unfortunately, recent studies predicting the global distribution of the disease and the demonstration of melioidosis endemicity in Puerto Rico have not increased recognition of the disease by health professionals in this region. Furthermore, a lack of both diagnostic capacity and awareness of the disease has resulted in a limited number of studies that have attempted to accurately determine its prevalence and geographical distribution. In this review, a summary of reported cases in the countries of this region are presented, as well as recommendations to increase the diagnosis and awareness of the disease as an important public health problem in Mexico, Central America, and the Caribbean islands.
... The first South American case of ZIKV was reported by the national authorities of Chile in Easter Island in February 2014 (Tognarelli et al. 2016), then Brazil in 2015 (Zanluca et al. 2015), and Argentina (Ministerio de Salud de la Naci on 2016). The recent finding of natural infection of monkeys by ZIKV (Favoretto et al. 2016) in Brazil and by DENV in Puerto Rico (Hemme et al. 2016) indicates spillover from the infected human population and possibly the establishment of enzootic cycles. If this is followed by persistent transmission among these mammals of CHIKV, as occurs in Africa (Chevillon et al. 2008) and Asia (Apandi et al. 2009), containment will be very difficult and could create an epidemiological situation similar to YFV. ...
... In the United States, most intervention programs for arboviruses such as WNV attempt to suppress vector populations below levels where spillover transmission to humans remains infrequent. In Puerto Rico, nonhuman primates have serologically tested positive for DENV; however, it is not clear whether this shows enzootic transmission or virus spillover from humans to monkeys (Hemme et al. 2016). If a stable enzootic cycle exists between mosquitoes and other mammals such as nonhuman primates, the elimination of the virus may be improbable and recurrent emergence expected. ...
