Emergence of Human Arboviral Diseases in the Americas,2000

Abstract

In addition to individual or clusters of cases of human infections with arboviruses, the past 15 years has seen the emergence of newly recognized arboviruses and the re-emergence of others. Mentioned in this brief summary are Bourbon, Cache Valley, chikungunya, Heartland, Itaqui, Mayaro, Oropouche, Powassan, and Zika viruses, the latter being a remarkable occurrence.

Introduction

Zoonoses are diseases caused by pathogens that can be transmitted between animals and humans. The World Health Organization has defined an emerging zoonosis as one that is “newly recognized or newly evolved, or that has occurred previously but show an increase in incidence or expansion in geographical, host or vector range” (World Health Organization 2004). Since females of hematophagous arthropods (mosquitoes, ticks, midges, and other insects) take blood meals (hematophagous) to lay eggs, they also can become incidentally infected with viruses in the blood of their hosts. Infection of the arthropod host then can lead to infection of a host on which it subsequently feeds.

Such zoonotic cycles play an important role in introducing arboviruses to human populations. Maintenance of an epidemic cycle can then be sustained by arthropods involved in human-to-human virus transmission in urban cycles.

More than 60% of the ∼400 emerging infectious diseases that have been identified since 1940 are zoonotic (Taylor et al. 2001, Jones et al. 2008, Wang and Crameri 2014) and the emergence of zoonoses in humans appears to be a continuing, even increasing, dynamic (Morse et al. 2012). These may partly be due to an increasing human population density with its attendant increases in agricultural areas needed and other anthropogenic alterations.

To calculate a possible approximate prospective estimate of total viral diversity, Anthony et al. (2013) used the Indian flying fox (Pteropus giganteus) as an exemplar host. Using PCR with degenerate virus family-level primers and statistical analyses, they found that these bats might contain 58 viruses of nine virus families. From that proof-of-concept step, they extrapolated their results, taking into consideration the numerous mammalian species of the world, and found that there might be 320,000 undiscovered mammalian viruses. Such a complexity cannot be reviewed simply and so we here focus on only the arbovirus diseases that have emerged in this century. This is not unreasonable, given that most emerging zoonoses are caused by viruses and have originated in wildlife and that there already are >500 known arboviruses (https://wwwn.cdc.gov/arbocat/VirusBrowser.aspx). For our purposes, we began by using the Program to Monitor Emerging Diseases (Pmm-archives [Pmm-A]; www.promedmail.org/) and used its search engine, using words such as “virus,” “arbovirus,” and “emerging,” and limited our search to the Americas and to the years from 2005 to 2016, so that our results would be focused and reflect recent findings. Other literature sources, including PubMed (www.ncbi.nlm.nih.gov/pubmed) and the U.S. Centers for Disease Control website (www.cdc.gov), also were used.

Emergences

Many of the hundreds of arboviruses that have been found in the Western Hemisphere cause human disease but detecting them is not a common occurrence, except fortuitously during clinical investigations. Infections with most of these viruses cause no illness or cause mild illness in general characterized by fever, headache, and malaise. Others may cause severe illness in individual cases or even in clusters of cases or in outbreaks and epidemics. These include viruses such as Eastern equine encephalitis virus (EEEV), Western equine encephalitis virus (WEEV), Venezuelan equine encephalitis virus (VEEV), St. Louis encephalitis virus (SLEV), California serogroup viruses, such as La Crosse virus (LACV), Jamestown Canyon virus (JCV), Snowshoe hare, and others in North America, as well as Oropouche, Mayaro, Caraparu, Guama and many others in South America.

In the past, WEEV was shown to cause extensive equid epizootics and concurrent human cases in North America. However, few such cases have been recorded recently, possibly due to equid vaccination programs and due to human interventions (insecticide spraying programs) and human lifestyle changes (air conditioning). EEEV is even less frequently found than is WEEV as a cause of equid and human illnesses, although at least some few cases of each are found every year. Fortunately, most individuals infected with EEEV are asymptomatic; in symptomatic cases, the case fatality rate is about 33%, and survivors have serious brain damage. Small, and possibly significant, nucleotide sequence differences in North, Central, and South Americas are likely responsible for the lower attack rates of these viruses, the further south they are found.

West Nile virus (WNV) (family Flaviviridae, genus Flavivirus) was first detected in the Americas in New York City in 1999 and has since spread to South America and may be in competition to some degree with the closely related SLEV. SLEV was only detected in 67 neuroinvasive disease cases between 2004 and 2013, whereas the mean number of neuroinvasive cases of infection with this virus from 1964 to 2010 had been about 100 per annum but ranged from 2 to 1967. In South America, human infections with SLEV have been detected in Peru, Argentina, and Brazil. In Brazil, in 2013, an isolate of SLEV was made from a human (Vedovello et al. 2015). This finding has provided an opportunity to accumulate more information regarding the origin and epidemiology of this virus, which is found infrequently in South America but does not seem to be emerging there.

Neuroinvasive disease caused by LACV (family Bunyaviridae, genus Orthobunyavirus, California serogroup) occurs mainly in the southeastern United States. and in its Upper Midwest. It is endemic to those locations (mean of ca. 80–100 cases per annum) and may cause serious central nervous system disease, principally in humans <15 years old. Illnesses caused by other California serogroup viruses are rare or have not been documented. Very rarely, however, Jamestown Canyon and Snowshoe hare California serogroup viruses have been documented to cause human illnesses but they do not appear to be emerging.

The four dengue viruses (family Flaviviridae, genus Flavivirus) will not be mentioned further, other than to say that dengue fever and some cases of dengue hemorrhagic fever is continually emerging and has been for the past 50 or so years. Possibly the most important of the arboviruses, descriptions of the epidemiologic situation with regard to the dengue viruses, progress in developing vaccines, clinical aspects, molecular characteristics, and so on, have been published (Rodriguez-Roche et al. 2016, Rothman and Ennis 2016, Tavakolipoor et al. 2016). Other clinically significant arboviruses, such as yellow fever virus, occur from time to time and also are not newly relevant. As an excellent vaccine is available for prophylaxis, the occurrence of yellow fever cases probably can be attributed to governmental failure.

Bourbon virus

In 2014, a previously healthy male >50-year-old farmer from Bourbon County, Kansas, USA, became ill with nausea, weakness, and diarrhea. That spring he had been fed upon by multiple ticks on his property. By the next day, he had developed fever, anorexia, chills, headache, myalgia and arthralgia. When he did not improve after treatment with doxycycline, he was hospitalized. His condition declined and he died 11 days after illness onset (Kosoy et al. 2015). An orthomyxovirus (family Orthomyxoviridae, genus Thogotovirus) was isolated in vero cell cultures and identified by RT-PCR. Another infection with this virus was detected in a human in nearby Oklahoma; that patient survived (Pmm-A 20150528.3390595). It is unknown at this time how widespread this virus is, what its likely tick vector is, and whether these two cases represent rare or hitherto undiagnosed infections. Other viruses of the genus Thogotovirus are tickborne and have only rarely been shown to cause human illnesses.

Cache Valley virus

Originally isolated from Culiseta inornata mosquitoes in Utah, USA (Holden and Hess 1959), Cache Valley virus (CVV; family Bunyaviridae, genus Orthobunyavirus, Bunyamwera group) has been found essentially throughout North America and has been reported to occur elsewhere in the Americas, but these may reflect the presence of viruses closely related to CVV. Antibody to CVV is commonly detected in small mammals, and sometimes detected in healthy humans. Congenital anomalies (arthrogryposis and hydranencephaly), abortions, and stillbirths occurred in CVV-infected sheep in west Texas in the winter of 1986–1987 (Edwards et al. 1989).

Subsequent outbreaks of this virus in sheep in Texas and elsewhere in the United States supported and extended these findings, but it was not until 1995 that Cache Valley virus was isolated from a previously healthy human in North Carolina, USA (Sexton et al. 1997). The 28-year-old male patient had been fed upon by numerous mosquitoes 2 weeks before the onset of his illness (myalgias, fever, chills, nausea. and headache). As his disease progressed (vomiting, confusion, tachycardia, fever, maculopapular rash, bilateral conjunctivitis, meningismus), renal failure and further central nervous system involvement were observed. The patient died of pulmonary complications 8 months after the onset of his illness. CVV was isolated from a blood sample collected from the patient a week after onset and from a cerebrospinal fluid sample collected 9 days after onset.

In late 2003, a 41-year-old male in Wisconsin became acutely ill with signs and symptoms similar to the earlier described case and was hospitalized. His health improved over the next few days and he was released from the hospital and discharged. CVV was isolated from a cerebrospinal fluid sample taken at hospital admission (Campbell et al. 2006).

Cerebrospinal fluid of a third patient, this one a 63-year-old woman living in northern New York with an illness comprising similar signs and symptoms of the previous cases, yielded an isolate of CVV; a diagnostically significant rise in neutralizing antibody titer was detected between acute- and convalescent-phase serum samples from the patient. She was released from the hospital but continued to have central nervous system problems even a year afterward (Nguyen et al. 2013).

One other case of human disease due to Bunyamwera group viruses has been reported from North America. An encephalitis case in Indiana was suggested to have been caused by Tensaw virus in 1964, but the known range of Tensaw virus does not include Indiana and other useful epidemiologic information was not available, so that the validity of this diagnosis is unproven (Campbell et al. 2006). Because of the wide geographic range of this virus in North America and the occurrence of antibody to it in humans (Calisher et al. 1986), the patient likely had an infection with a related bunyavirus.

It is likely that sporadic cases of infections caused by CVV and other enzootic, commonly detected viruses will continue to be found but they are not considered emerging. One study proposed that Bunyamwera serogroup viruses may be responsible for human congenital defects of the central nervous system in the United States (Calisher and Sever 1995). Conversely, it may be that such infections, as are so many others, are unrecognized and underreported.

Oropouche virus

Oropouche virus (OROV), a member of the family Bunyaviridae, genus Orthobunyavirus, was initially isolated from blood samples of febrile people in Trinidad and Tobago in the 1950s. In the early 1960s, it was isolated in Brazil and shown to be responsible for an epidemic of febrile illness in Belem, Para State (Pinheiro et al. 1962). In the following years, several outbreaks and epidemics of OROV were reported in the Brazilian Amazon region, as well as in Peru, Panama, Trinidad and Tobago. In Brazil, it is estimated that half a million people were infected. OROV causes an illness characterized by sudden onset, with fever, headache, retroocular pain, and myalgia. Usually, this clinical picture lasts for 4–5 days.

During large epidemics, OROV was associated with more severe clinical presentations and from some patients the virus was isolated from the cerebrospinal fluid clinically diagnosed with aseptic meningitis. Recent episodes of OROV fever have been reported in Iquitos (Peru) and Magalhães Barata, Pará State, Brazil (Vasconcelos et al. 2009). In 2000, the existence of three genotypes of OROV was demonstrated and confirmed by phylogeographic and evolutionary analyses (Saeed et al. 2000) and a fourth genotype identified in Manaus, Amazonas State (Vasconcelos et al. 2011). Interestingly, all four genotypes have been found only in Brazil.

The spread of OROV into urban settings is facilitated by midges (Culicoides paraensis), but the maintenance (jungle) cycle remains to be determined. In this century, OROV has been isolated from nonhuman primates, including capuchin monkeys (Sapajus spp.) and black-and-gold howler monkeys (Alouatta caraya) in Mato Grosso do Sul (Batista et al. 2013), as well as from black-tufted marmosets (Callithrix penicillata) on two different occasions in Minas Gerais State, showing the potential of OROV to spread in the most populated areas of southeastern Brazil (Nunes et al. 2005, Tilson-Lunel et al. 2015).

Chikungunya virus

First isolated from a febrile patient with arthralgias in Tanzania, chikungunya virus (CHIKV) (family Togaviridae, genus Alphavirus) has caused individual cases, clusters of cases, and huge epidemics of disease in Africa, Asia, and the Indian subcontinent.

In 1999–2000, there was a large outbreak of CHIKV disease in humans in the Democratic Republic of the Congo, and in 2007, there was an outbreak in Gabon. Beginning early in 2005, a major outbreak of disease caused by CHIKV was recognized in islands of the Indian Ocean and a large number of imported cases in Europe were associated with this outbreak, mostly in 2006 when the Indian Ocean epidemic was at its peak. A large outbreak of CHIKV occurred in India in 2006 and 2007. It was estimated that about 2 million infections had occurred. Several other countries in Southeast Asia were also affected.

Since 2005, India, Indonesia, Maldives, Myanmar, and Thailand have reported more than 1.9 million cases. In 2007, transmission was reported for the first time in Europe, in a localized outbreak in northeastern Italy. There were 197 cases recorded during this outbreak and it confirmed that mosquito-borne outbreaks were being sustained by Aedes albopictus mosquitoes in Europe.

By December 2013, France had reported two laboratory-confirmed autochthonous cases in the French part of the Caribbean island of St Martin. Since then, local transmission has been confirmed in more than 43 countries and territories in the Americas. This was the first documented outbreak of CHIKV disease with autochthonous transmission in the Americas. According to the Pan American Health Organization, as of January 2016, more than 1.5 million confirmed or suspect cases of chikungunya have been recorded in the Western Hemisphere (www.paho.org/hq/index.php?option=com_topics&view=article&id=343&Itemid=40931&lang=en). During the same period, 71 deaths were attributed to this disease.

Three distinct CHIKV genotypes have been recognized, the most widespread being the Asian genotype, which has been responsible for the majority of cases in the Caribbean, and in Central and South Americas, including Brazil (Teixeira et al. 2015). A 2014 study showed that the East/Central/South African genotype of CHIKV had caused an extensive epidemic involving both north and northeastern Brazil (Nunes et al. 2015).

In October 2014, France confirmed four cases of a locally acquired CHIKV infection in Montpellier, France, and in late 2014, outbreaks were reported in the Pacific islands. Currently, a CHIKV outbreak is occurring in the Cook Islands and Marshall Islands, while the number of cases in American Samoa, French Polynesia, Kiribati, and Samoa has decreased. Canada, Mexico, and the United States have recorded many imported cases and locally acquired CHIKV infections have been identified in Florida (Kendrick et al. 2014).

Before 2006, CHIKV disease was rarely identified in travelers returning to the Americas. In late 2013, the first local transmission of CHIKV in the Americas was identified in Caribbean countries. Beginning in 2014, CHIKV disease cases were reported among U.S. travelers returning from affected areas in the Americas, and local transmission was identified in Puerto Rico and the U.S. Virgin Islands. At this time, imported cases of CHIKV infection have been reported in all states of the United States as well as all other countries in the Western Hemisphere with the exception of Canada, Cuba, Argentina, Chile, and Uruguay. This has been and is a true epidemic extension of this virus and its attendant disease. Fortunately, most cases are mild, but more than a million human infections are estimated to have occurred in the Western Hemisphere.

Heartland virus

Human infections with a hitherto unrecognized bunyavirus, Heartland virus (HRTV) (family Bunyaviridae, genus Phlebovirus), named for the institute where the patients were treated, were diagnosed between 2012 and 2013 by virus isolation and serology in two humans in Missouri (McMullan et al. 2012). Subsequent studies detected six more cases in Missouri and one in Tennessee (Pastula et al. 2014). Of the first six recognized case patients, all were males, 60 years old or older.

Because of the seasonality of these infections (May–September), a similar constellation of signs and symptoms (fever, thrombocytopenia, leukopenia; recorded symptoms also included fatigue, anorexia, headache, nausea, and myalgia or arthralgia), participating in outdoor activities for several hours each day, and tick bites (5/6) in the 14 days preceding their illness onsets, it was assumed that the cause of their illnesses was a virus transmitted by ticks. Indeed, confirmation of the infections was made by RT-PCR detection of Heartland viral RNA, rise in antibody by neutralization test, or both. HRTV was isolated from Lone Star ticks (Amblyomma americanum) but not from other ticks or from mosquitoes collected in appropriate areas (Savage et al. 2013).

Other surveys suggest that human disease caused by HRTV is relatively rare, although with few laboratories testing for it. It should be noted that, however, a human death attributed to HRTV occurred in Oklahoma in 2014 (www.ok.gov/health/Organization/Office_of_Communications/News_Releases/2014_News_Releases/Oklahoma_State_Health_Department_Confirms_First_Case_and_Death_of_Heartland_Virus.html) and antibody to HRTV, or a close relative of it, has been detected in deer, raccoons, coyotes, and moose in 13 states, from Texas to North Carolina and Florida to Maine. It has been suggested that clinicians in the relevant geographic areas be aware of the features of infection with this virus. At this time, HRTV and severe fever with thrombocytopenia syndrome virus, detected in ticks in Asia, are the only two tickborne phleboviruses recognized to cause human illnesses (Yu et al. 2011).

Iquitos virus

A reassortant orthobunyavirus, Iquitos virus, containing the S and L segments of OROV (Simbu serogroup), a known human pathogen, and the M segment of a newly recognized Simbu antigenic group orthobunyavirus was first isolated from a febrile patient in Peru, then shown to be the etiologic agent of outbreaks of OROV disease in the same area (Aguilar et al. 2011). Midges (C. paraensis) and mosquitoes of various species are the likely vectors. Given the scores of orthobunyaviruses in Brazil and elsewhere, it would not be surprising to see more bunyavirus reassortant emergences in those areas. Indeed, what with the circulation of a multitude of alphaviruses, flaviviruses, bunyaviruses, and other viruses that cause mild 3-day fevers with rash, such illnesses may be greatly underdiagnosed throughout both hemispheres.

Mayaro virus

Isolated from a human in Trinidad in 1954, Mayaro virus (family Togaviridae, genus Alphavirus) infections have been detected in humans in Brazil, Bolivia, Colombia (https://wwwn.cdc.gov/arbocat/VirusBrowser.aspx), French Guiana, Peru, Suriname, Venezuela (Auguste et al. 2015), and even from a northbound migrating bird, an orchard oriole (Icterus spurius) netted in Louisiana (Calisher et al. 1974). The disease is characterized by fever, headache, retro-orbital pain, rash, and arthralgia, which is long term in more than half the patients; an increase in proinflammatory cytokines (IL-13, IL-7, and vascular endothelial growth factor [VEGF]) has been correlated with persistent arthralgias (Santiago et al. 2015).

Canopy-dwelling mosquitoes, principally Haemagogus spp., but also from mosquitoes of many other species, and forest-dwelling nonhuman primates probably comprise the Mayaro virus enzootic transmission cycle and, consequently, infection and seropositivity to this virus in humans are largely associated with forest workers and hunters. Single cases, clusters of cases, and large epidemics have been reported through the years (Pinheiro et al. 1981, Powers et al. 2006).

In 2010, an outbreak of Mayaro virus disease occurred in Venezuela (Auguste et al. 2015) and intermittently, cases or clusters of cases occur in rural Amazonia and elsewhere in South America, but urban outbreaks have not been recognized (Azevedo et al. 2009), likely because the enzootic vectors are not present in those areas. Although not meeting the strict definition of an emerging disease, Mayaro virus infection may yet adapt to a condition in which it does.

Powassan virus

This virus (family Flaviviridae, genus Flavivirus) was first isolated from human tissues collected in 1958 at autopsy from a case patient in Ontario, Canada (McLean and Donohue 1959). Subsequent isolates were obtained from ticks, mostly Ixodidae, mainly Ix. cookei, collected in the states of South Dakota, Massachusetts, New York, and Connecticut. In 1962, Russian investigators isolated Powassan virus from humans and from Ix. persulcatus ticks in western Siberia (Chumakov 1963). A closely related subtype of Powassan virus, named “deer tick virus,” was isolated from Ix. scapularis, conspecific with Ix. dammini, collected in Massachusetts and Connecticut (Telford et al. 1997). Although it was seen as an infrequently observed cause of human infections, within the past 15 years, the number of cases of encephalitis caused by Powassan virus and its deer tick virus subtype has increased (Hinten et al. 2008).

Deer ticks feed on deer (Odocoileus virginianus) and deer populations have, by one estimate alone (http://wildlifecontrol.info/deer/Pages/Populations.aspx), increased 40-fold in the past 100 years and are continuing to increase in areas where both prototype Powassan virus and variant deer-tick virus occur, so it is not surprising that Powassan virus disease is being increasingly diagnosed. Increased awareness of and testing for West Nile virus infections in North America also are likely reasons for this apparent disease increase in the northern tier of the United States, extending southward in the United States.

Zika virus

A truly eye-opening pandemic, “a tsunami,” of Zika virus (family Flaviviridae, genus Flavivirus) has been occurring for the past 3 years. Isolated from a sentinel rhesus monkey (Macaca mulatta) in 1947 in Uganda (Dick et al. 1952), Zika virus subsequently was isolated from humans in other African countries and antibody to it was detected in humans in Africa and in Asia (https://wwwn.cdc.gov/arbocat/VirusBrowser.aspx), but it was considered a rather benign virus, causing only mild infections. As antibody to a flavivirus might result from infection with a heterologous flavivirus, it was not until Zika virus was isolated from Aedes aegypti mosquitoes in Malaysia that its presence in Asia was confirmed (Marchette et al. 1969).

Since then, it has been shown that Zika virus may be transmitted by mosquitoes of various Aedes species and that nonhuman primates serve as reservoirs or intermediate hosts. Human clinical infections caused by Zika virus are generally self-limiting febrile illnesses; 3- to 12-day incubation period, followed by 4 to 7 days of illness, characterized by exanthema and arthralgia, closely resembling dengue and chikungunya fevers, both of which also are vectored by Aedes aegypti mosquitoes. Signs and symptoms may also include maculopapular rash, fever, arthralgia, myalgia, headache, and conjunctivitis; notably, in 2013, a 20-fold increase of Guillain-Barré syndrome incidence was noted in patients with Zika virus infections in French Polynesia.

Reports of Zika virus infections had been sparse (14 cases in about 50 years) until 2007, when an epidemic of disease caused by this virus was recognized on Yap Island, Federated States of Micronesia (Duffy et al. 2009). Isolated cases and clusters of cases continued to occur in tourists returning from or within Asia and in residents of endemic countries, with increasing evidence of the spread of this disease throughout many parts of Asia. Zika virus infections have been diagnosed in travelers returning from Pacific islands and Africa to the Americas and vice versa. Person-to-person sexual transmission of the virus from a Zika virus-infected individual returning to the United States from Senegal in 2008 has been reported (Foy et al. 2011).

In 2013, during a Zika virus outbreak in Tahiti, a patient there with low-grade fever and arthralgia who was clinically diagnosed as having a Zika virus infection developed hematospermia; Zika virus was isolated from his semen and urine but not blood (Musso et al. 2015). Increasingly, sexual transmission of this virus is being recognized.

In 2014, however, an epidemic of Zika virus disease occurred among residents of Easter Island, Chilean Pacific territory (Tognarelli et al. 2016). Analysis of NS5 genes found that the most closely related strains of the virus responsible for this epidemic were those from French Polynesia, with nearly 100% nucleotide and amino acid identity. Likewise, when the French Polynesian strain of Zika virus was detected in Brazil (Campos et al. 2015), then also in Suriname, Colombia, Dominican Republic, Mexico, Paraguay, and El Salvador, it became clear that this virus was causing an on-going pandemic.

Unfortunately, an increase in birth defects, mainly microcephaly, has been reported in the offspring of Brazilian patients with Zika virus infections (Pmm-A 20151121.3808514). Recently, the Instituto Evandro Chagas (Ananindeua, Brazil) has isolated Zika virus from three fatal cases (Vasconcelos, unpublished data). A 35-year-old man suffering systemic lupus erythematosus and rheumatoid arthritis and taking steroids for many years died with a hemorrhagic fever. Real-time RT-PCR was positive with his brain tissue and with liver, heart, lung, spleen and kidney tissues and Zika virus was isolated from pooled visceral tissue.

The second case was that of a 16-year-old girl with a febrile disease whose clinical condition worsened rapidly; she died after a month of illness. Zika virus was isolated from a serum sample collected 7 days postonset. The third case was an infant who died a few hours after birth. Similar to the first case, Zika viral RNA was detected in brain tissue, cerebrospinal fluid, and all visceral tissues examined; the virus also was isolated from pooled visceral tissues. Virus in all three cases was characterized as Asian genotype (related to the French Polynesian subclade).

More recently, a correlation between Guillan-Barré syndrome and the presence of Zika virus was demonstrated by the Brazilian Ministry of Health (www.portalsaude.gov.br). Zika virus was detected by real-time PCR in the cerebrospinal fluid of patients previously diagnosed with Zika virus fever. Macular atrophy has also been associated with Zika virus in utero infections in Brazil (Ventura et al. 2016). As always with such surprising outbreaks, additional studies are necessary to confirm or deny these associations.

Summary

Emergence of newly recognized arboviruses and re-emergence of recognized arboviruses in the Americas, as elsewhere, are continuing problems. Often, there is a delay in identifying these viruses for lack of immediate recognition that they are new, have serious potential, or because of lack of experienced personnel due to budgetary changes; reinventing the wheel is not efficient. As human movements and man-made ecologic changes alter or otherwise impact the epidemiology of arboviruses and other viruses, this situation will only worsen and the burden on human populations is likely to increase.

Footnotes

Author Disclosure Statement

No competing financial interests exist.

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Emergence of Human Arboviral Diseases in the Americas,2000–2016

Abstract

Introduction

Emergences

Bourbon virus

Cache Valley virus

Oropouche virus

Chikungunya virus

Heartland virus

Iquitos virus

Mayaro virus

Powassan virus

Zika virus

Summary

Footnotes

Author Disclosure Statement

References