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Zika virus, vectors, reservoirs, amplifying hosts, and their potential to spread worldwide: what we know and what we should investigate urgently

Open AccessPublished:May 18, 2016DOI:https://doi.org/10.1016/j.ijid.2016.05.014

      Highlights

      • Zika virus (ZIKV) is widely distributed among animal hosts and vectors.
      • Its circulation in a wide range of animals and vectors in West Africa has been correlated with the emergence of recombinants.
      • Aedes albopictus is becoming established as a competent vector, having invaded Central Africa, the Mediterranean, and parts of Central and Northern Europe.
      • Antibodies against the virus have been detected in domestic sheep and goats, horses, cows, ducks, rodents, bats, orangutans, and carabaos in Southeast Asia, separate from the strains of the virus isolated from monkeys in Africa.
      • In Africa, ZIKV has been isolated in mosquitoes of the genera Aedes, Anopheles, and Mansonia.

      Summary

      Objectives

      The widespread epidemic of Zika virus infection in South and Central America and the Caribbean in 2015, along with the increased incidence of microcephaly in fetuses born to mothers infected with Zika virus and the potential for worldwide spread, indicate the need to review the current literature regarding vectors, reservoirs, and amplification hosts.

      Vectors

      The virus has been isolated in Africa in mosquitoes of the genera Aedes, Anopheles, and Mansonia, and in Southeast Asia and the Pacific area in mosquitoes of the genus Aedes. Aedes albopictus has invaded several countries in Central Africa and all Mediterranean countries, and continues to spread throughout Central and Northern Europe. The wide distribution of the virus in animal hosts and vectors favors the emergence of recombinants.

      Animal hosts

      The virus has been isolated in monkeys, and antibodies have been detected in domestic sheep, goats, horses, cows, ducks, rodents, bats, orangutans, and carabaos.

      Conclusions

      It is a public health imperative to define the domestic and wild animal reservoirs, amplification hosts, and vector capacity of the genera Aedes, Anopheles, and Mansonia. These variables will define the geographic distribution of Zika virus along with the indicated timing and scale of the environmental public health interventions worldwide.

      Keywords

      1. Introduction

      A widespread epidemic of Zika virus (ZIKV) infection was reported in 2015 in Central and South America and the Caribbean. This epidemic was associated with an increased incidence of microcephaly in fetuses born to mothers infected with ZIKV, with Brazil being the country most affected by both epidemics.
      • Ventura C.V.
      • Maia M.
      • Ventura B.V.
      • Linden V.V.
      • Araujo E.B.
      • Ramos R.C.
      • et al.
      Ophthalmological findings in infants with microcephaly and presumable intra-uterus Zika virus infection.
      • Petersen E.
      • Wilson M.E.
      • Touch S.
      • McCloskey B.
      • Mwaba P.
      • Bates M.
      • et al.
      Unexpected and rapid spread of Zika virus in the Americas—implications for public health preparedness for mass gatherings at the 2016 Brazil Olympic Games.
      • Mlakar J.
      • Korva M.
      • Tul N.
      • Popovic M.
      • Poljsak-Prijatelj M.
      • Mraz J.
      • Kolenc M.
      • et al.
      Zika virus associated with microcephaly.
      • Rubin E.J.
      • Greene M.F.
      • Baden L.R.
      Zika virus and microcephaly.
      This rare, devastating, and untreatable complication of the fetus was declared a public health emergency of international concern (PHEIC).
      • Ventura C.V.
      • Maia M.
      • Ventura B.V.
      • Linden V.V.
      • Araujo E.B.
      • Ramos R.C.
      • et al.
      Ophthalmological findings in infants with microcephaly and presumable intra-uterus Zika virus infection.
      • Petersen E.
      • Wilson M.E.
      • Touch S.
      • McCloskey B.
      • Mwaba P.
      • Bates M.
      • et al.
      Unexpected and rapid spread of Zika virus in the Americas—implications for public health preparedness for mass gatherings at the 2016 Brazil Olympic Games.
      • Mlakar J.
      • Korva M.
      • Tul N.
      • Popovic M.
      • Poljsak-Prijatelj M.
      • Mraz J.
      • Kolenc M.
      • et al.
      Zika virus associated with microcephaly.
      • Rubin E.J.
      • Greene M.F.
      • Baden L.R.
      Zika virus and microcephaly.
      The neurotropism of the virus was recognized early,
      • Dick G.W.
      • Kitchen S.F.
      • Haddow A.J.
      Zika virus. I. Isolations and serological specificity.
      and this has been evident in the recent rise in microcephaly incidence in Brazil .
      • Mlakar J.
      • Korva M.
      • Tul N.
      • Popovic M.
      • Poljsak-Prijatelj M.
      • Mraz J.
      • Kolenc M.
      • et al.
      Zika virus associated with microcephaly.
      • Rubin E.J.
      • Greene M.F.
      • Baden L.R.
      Zika virus and microcephaly.
      • Schuler-Faccini L.
      • Ribeiro E.M.
      • Feitosa I.M.
      • Horovitz D.D.
      • Cavalcanti D.P.
      • Pessoa A.
      • et al.
      Brazilian Medical Genetics Society—Zika Embryopathy Task Force. Possible association between Zika virus infection and microcephaly—Brazil, 2015.
      The virus has been found in the amniotic fluid of two pregnant women with fetuses suffering a reduction in the circumference of the head.
      • Schuler-Faccini L.
      • Ribeiro E.M.
      • Feitosa I.M.
      • Horovitz D.D.
      • Cavalcanti D.P.
      • Pessoa A.
      • et al.
      Brazilian Medical Genetics Society—Zika Embryopathy Task Force. Possible association between Zika virus infection and microcephaly—Brazil, 2015.
      The virus has also been found in the central nervous system (CNS) of fetuses,
      • Mlakar J.
      • Korva M.
      • Tul N.
      • Popovic M.
      • Poljsak-Prijatelj M.
      • Mraz J.
      • Kolenc M.
      • et al.
      Zika virus associated with microcephaly.
      • Rubin E.J.
      • Greene M.F.
      • Baden L.R.
      Zika virus and microcephaly.
      with negative tests excluding other congenital infections.
      • Schuler-Faccini L.
      • Ribeiro E.M.
      • Feitosa I.M.
      • Horovitz D.D.
      • Cavalcanti D.P.
      • Pessoa A.
      • et al.
      Brazilian Medical Genetics Society—Zika Embryopathy Task Force. Possible association between Zika virus infection and microcephaly—Brazil, 2015.
      Thirty-two countries and territories of the Americas are affected by ZIKV, in addition to Rio de Janeiro, Brazil, where the Olympics and Paralympics are due to be held in August 2016; this poses a threat to international travelers and the local host-country residents .
      • Petersen E.
      • Wilson M.E.
      • Touch S.
      • McCloskey B.
      • Mwaba P.
      • Bates M.
      • et al.
      Unexpected and rapid spread of Zika virus in the Americas—implications for public health preparedness for mass gatherings at the 2016 Brazil Olympic Games.
      Local transmission has not been observed in Europe yet, and there is a global alert for travelers returning from endemic countries with symptoms consistent with ZIKV infection.
      The immediate public health measures feasible at present, in the absence of a vaccine, are interventions relevant to the vector and a better understanding of the wide and unknown range of possible amplification hosts. Two main concerns prompted this exhaustive review of the literature: the historical paradigm of the introduction of yellow fever virus from Africa to the Americas, where it adapted to local sylvatic vectors and primates,
      • Prata A.
      Yellow fever.
      and the fact that we do not yet know which could be the competent vectors or amplifying hosts of ZIKV in temperate climate regions, thus hampering any future surveillance and intervention control programs. The range of vectors and animals in which the virus has been detected worldwide was reviewed in order to assess the likelihood of an established circulation of the virus in novel areas.

      2. Epidemiology

      ZIKV is an emerging vector-borne pathogen that was first isolated in 1947 in a sentinel rhesus macaque monkey and again in 1948 from a pooled specimen of Aedes africanus mosquitoes from the Zika Forest in Uganda.
      • Dick G.W.
      • Kitchen S.F.
      • Haddow A.J.
      Zika virus. I. Isolations and serological specificity.
      During the years 1947 through 2007, only serological data, entomological data, and the diagnosis of 14 human cases with viral isolation or serology were reported from Asia and Africa.
      • Fagbami A.H.
      Zika virus infections in Nigeria: virological and seroepidemiological investigations in Oyo State.
      • Darwish M.A.
      • Hoogstraal H.
      • Roberts T.J.
      • Ahmed I.P.
      • Omar F.
      A sero-epidemiological survey for certain arboviruses (Togaviridae) in Pakistan.
      • Haddow A.J.
      • Williams M.C.
      • Woodall J.P.
      • Simpson D.I.
      • Goma L.K.
      Twelve isolations of Zika virus from Aedes (Stegomyia) africanus (Theobald) taken in and above a Uganda Forest.
      • Marchette N.J.
      • Garcia R.
      • Rudnick A.
      Isolation of Zika virus from Aedes aegypti mosquitoes in Malaysia.
      • McCrae A.W.
      • Kirya B.G.
      Yellow fever and Zika virus epizootics and enzootics in Uganda.
      • Saluzzo J.F.
      • Ivanoff B.
      • Languillat G.
      • Georges A.J.
      [Serological survey for arbovirus antibodies in the human and simian populations of the South-East of Gabon (author's transl)].
      It has been speculated that among those human cases, a few may have represented an unrecognized outbreak. One unrecognized outbreak took place in 1977–1978 in Indonesia.
      • Olson J.G.
      • Ksiazek T.G.
      • Suhandiman
      • Triwibowo
      Zika virus, a cause of fever in Central Java, Indonesia.
      • Olson J.G.
      • Ksiazek T.G.
      • Gubler D.J.
      • Lubis S.I.
      • Simanjuntak G.
      • Lee V.H.
      • et al.
      A survey for arboviral antibodies in sera of humans and animals in Lombok, Republic of Indonesia.
      The first outbreak outside of Africa and Asia occurred in 2007, on Yap Island in the Federated States of Micronesia, with 49 confirmed cases and 73% of residents aged ≥3 years infected according to IgM seropositivity.
      • Lanciotti R.S.
      • Kosoy O.L.
      • Laven J.J.
      • Velez J.O.
      • Lambert A.J.
      • Johnson A.J.
      • Stanfield S.M.
      • Duffy M.R.
      Genetic and serologic properties of Zika virus associated with an epidemic, Yap State, Micronesia, 2007.
      • Duffy M.R.
      • Chen T.H.
      • Hancock W.T.
      • Powers A.M.
      • Kool J.L.
      • Lanciotti R.S.
      • et al.
      Zika virus outbreak on Yap Island, Federated States of Micronesia.
      There are limitations to the seroprevalence studies resulting from the cross-reactive nature of ZIKV with dengue and other flaviviruses. However, IgM antibodies against dengue virus persist for up to 12 weeks, and the specimens for the IgM measurement were collected during a 12-week period from April 1 through July 31, 2007. During this time, the specimens had been collected within 10 days from symptom onset. They tested positive only for ZIKV RNA and not for dengue or other flavivirus RNA.
      • Duffy M.R.
      • Chen T.H.
      • Hancock W.T.
      • Powers A.M.
      • Kool J.L.
      • Lanciotti R.S.
      • et al.
      Zika virus outbreak on Yap Island, Federated States of Micronesia.
      From 2007 through 2013, no new instances of human seropositivity or disease were reported. In 2013, the virus reemerged in French Polynesia, and from 2013 through 2014, it disseminated to the Cook Islands, New Caledonia, Easter Island, and throughout the Pacific.
      • Musso D.
      • Nilles E.J.
      • Cao-Lormeau V.M.
      Rapid spread of emerging Zika virus in the Pacific area.
      French Polynesia reported 396 epidemiologically confirmed cases and 29 000 suspected cases.
      • Ioos S.
      • Mallet H.P.
      • Leparc Goffart I.
      • Gauthier V.
      • Cardoso T.
      • Herida M.
      Current Zika virus epidemiology and recent epidemics.
      The virus has been isolated or has had its nucleic acid extracted by PCR and then sequenced from samples collected in Southeast Asia (e.g., Thailand, Indonesia, Cambodia
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      • Hermann L.
      • Thaisomboonsuk B.
      • Rutvisuttinunt W.
      • Klungthong C.
      • Chinnawirotpisan P.
      • et al.
      Detection of Zika virus infection in Thailand, 2012–2014.
      • Kwong J.C.
      • Druce J.D.
      • Leder K.
      Zika virus infection acquired during brief travel to Indonesia.
      • Heang V.
      • Yasuda C.Y.
      • Sovann L.
      • Haddow A.D.
      • Travassos da Rosa A.P.
      • Tesh R.B.
      • Kasper M.R.
      Zika virus infection, Cambodia, 2010.
      ). All strains collected in Asia and the Pacific belong to the Asian lineage and are closely related, indicating that the virus was present in the area for several years but remained undetected, as the clinical manifestations resemble those of other known endemic arboviruses such as dengue virus and chikungunya virus.
      • Buathong R.
      • Hermann L.
      • Thaisomboonsuk B.
      • Rutvisuttinunt W.
      • Klungthong C.
      • Chinnawirotpisan P.
      • et al.
      Detection of Zika virus infection in Thailand, 2012–2014.
      However, the possibility that the virus has spread to the Pacific and Southeast Asia successively, causing a wave of clinical disease and subsequent detection of the virus, cannot be excluded.
      • Buathong R.
      • Hermann L.
      • Thaisomboonsuk B.
      • Rutvisuttinunt W.
      • Klungthong C.
      • Chinnawirotpisan P.
      • et al.
      Detection of Zika virus infection in Thailand, 2012–2014.
      In March 2015, Brazil notified the World Health Organization of an illness compatible with but not suspected to be a ZIKV infection. Soon after, in May 2015, it documented the first confirmed ZIKV transmission in mainland South America, along with the assumption that the virus had been introduced to the country via the Va’a World Sprint Championship canoe race held in Rio de Janeiro in August 2014.
      • Zanluca C.
      • de Melo V.C.
      • Mosimann A.L.
      • Dos Santos G.I.
      • Dos Santos C.N.
      • Luz K.
      First report of autochthonous transmission of Zika virus in Brazil.
      Four Pacific countries participated (French Polynesia, New Caledonia, the Cook Islands, and Easter Island). The virus was subsequently transferred from the major cities across the country via the infected Brazilian participants and spectators who returned to their home towns.
      • Musso D.
      Zika virus transmission from French Polynesia to Brazil.
      The strain found in Brazil was phylogenetically closer to the strain in the French Polynesia outbreak of 2013–2014, with both belonging to the Asian lineage. It is estimated that 440 000 to 1.3 million cases had been reported as of December 2015.
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      • Dos Santos G.I.
      • Dos Santos C.N.
      • Luz K.
      First report of autochthonous transmission of Zika virus in Brazil.

      3. Virus

      ZIKV is an approximately 11-kb single-stranded, positive-sense ribonucleic acid (RNA) virus of the Flaviviridae family. It is related to dengue, West Nile, and Yellow fever viruses and is a member of the Spondweni serocomplex, whose transmission cycle consists mainly of vectors from the Aedes genus mosquitoes (A. furcifer, A. taylori, A. luteocephalus, and A. africanus) and monkeys.
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      • Freire C.C.
      • Iamarino A.
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      • Diallo M.
      • et al.
      Molecular evolution of Zika virus during its emergence in the 20th century.
      • Kuno G.
      • Chang G.J.
      • Tsuchiya K.R.
      • Karabatsos N.
      • Cropp C.B.
      Phylogeny of the genus Flavivirus.
      Phylogenetic analyses have revealed three lineages: two African lineages, i.e., the MR 766 cluster and the Nigerian cluster, and one Asian lineage (Table 1).
      • Lanciotti R.S.
      • Kosoy O.L.
      • Laven J.J.
      • Velez J.O.
      • Lambert A.J.
      • Johnson A.J.
      • Stanfield S.M.
      • Duffy M.R.
      Genetic and serologic properties of Zika virus associated with an epidemic, Yap State, Micronesia, 2007.
      • Cao-Lormeau V.M.
      • Roche C.
      • Teissier A.
      • Robin E.
      • Berry A.L.
      • Mallet H.P.
      • et al.
      Zika virus, French Polynesia, South Pacific, 2013.
      • Kuno G.
      • Chang G.J.
      Full-length sequencing and genomic characterization of Bagaza, Kedougou, and Zika viruses.
      Table 1Lineages of Zika virus
      1. African lineages (two clusters)2. Asian lineage
      a. MR 766 clusterOne Asian genotype
      b. Nigerian cluster
      All lineages share a common origin in Uganda early in the 20th century, from where it dispersed west to West Africa via two introductions and east to Southeast Asia and then to the Pacific as follows: (1) a relative of the MR 766 prototype strain was introduced from Uganda to Côte d’Ivoire in 1940 and from there to Senegal in 1985 resulting in the MR 766 lineage; (2) a relative of the Nigerian strain was introduced from Uganda to the Central African Republic and Nigeria around 1935, and from Nigeria to Senegal and Côte d’Ivoire around 1960, forming the Nigerian lineage; and (3) a ZIKV cluster was probably spread from Uganda to Malaysia in 1945, making its way to Micronesia sometime around 1960, where it formed the Asian lineage.
      • Faye O.
      • Freire C.C.
      • Iamarino A.
      • Faye O.
      • de Oliveira J.V.
      • Diallo M.
      • et al.
      Molecular evolution of Zika virus during its emergence in the 20th century.
      However, it is unknown whether to attribute this migration only to human and vector movements, or also to birds carrying the virus along migratory routes.
      Regarding the African lineages, the phylogenetic analysis of ZIKV strains collected from 1968 through 2002 in Senegal, Côte d’Ivoire, Burkina Faso, and the Central African Republic indicated that there are more recombinants than in other flaviviruses; however, they all clustered in the two African lineages, the MR 766 cluster and the Nigerian cluster.

      4. Transmission

      Transmission has been demonstrated to occur mostly via infected female mosquito vectors of the Aedes genus (Culicidae family). Transmission is mainly urban and sylvatic, with humans serving as primary amplification hosts in areas where there are no non-human primates.
      • Duffy M.R.
      • Chen T.H.
      • Hancock W.T.
      • Powers A.M.
      • Kool J.L.
      • Lanciotti R.S.
      • et al.
      Zika virus outbreak on Yap Island, Federated States of Micronesia.
      The latter constitute the amplification host in a sylvatic cycle.
      • Duffy M.R.
      • Chen T.H.
      • Hancock W.T.
      • Powers A.M.
      • Kool J.L.
      • Lanciotti R.S.
      • et al.
      Zika virus outbreak on Yap Island, Federated States of Micronesia.
      Mosquitoes, as hematophagus arthropods, acquire the virus via a blood meal, and they host it throughout their life-span without being affected. They transmit it to the next amplification host, i.e., their target during the next blood meal.
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      • Medlock J.M.
      • Van Bortel W.
      Public health significance of invasive mosquitoes in Europe.
      Other routes of transmission are sexual intercourse,
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      • Travassos da Rosa A.
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      • et al.
      Probable non-vector-borne transmission of Zika virus, Colorado, USA.
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      Zika virus in Brazil and the danger of infestation by Aedes (Stegomyia) mosquitoes.
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      Zika virus: following the path of dengue and chikungunya?.
      • Musso D.
      • Roche C.
      • Nhan T.X.
      • Robin E.
      • Teissier A.
      • Cao-Lormeau V.M.
      Detection of Zika virus in saliva.
      perinatal transmission from mother to fetus,
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      • Staples J.E.
      • Meaney-Delman D.
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      Interim guidelines for pregnant women during a Zika virus outbreak—United States, 2016.
      and blood transfusion.
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      • Grazzini G.
      Zika virus and the never-ending story of emerging pathogens and transfusion medicine.
      Breast feeding has not been reported as a mode of transmission.

      5. Clinical manifestations

      The majority of infections are subclinical, estimated to reach 81% of infected individuals. The clinical manifestations mimic those of other arboviral infections, e.g., dengue and the chikungunya endemic in tropical areas (West Africa, Southeast Asia, Pacific area, South America).
      • Petersen E.
      • Wilson M.E.
      • Touch S.
      • McCloskey B.
      • Mwaba P.
      • Bates M.
      • et al.
      Unexpected and rapid spread of Zika virus in the Americas—implications for public health preparedness for mass gatherings at the 2016 Brazil Olympic Games.
      • Duffy M.R.
      • Chen T.H.
      • Hancock W.T.
      • Powers A.M.
      • Kool J.L.
      • Lanciotti R.S.
      • et al.
      Zika virus outbreak on Yap Island, Federated States of Micronesia.
      • Heang V.
      • Yasuda C.Y.
      • Sovann L.
      • Haddow A.D.
      • Travassos da Rosa A.P.
      • Tesh R.B.
      • Kasper M.R.
      Zika virus infection, Cambodia, 2010.
      • Grard G.
      • Caron M.
      • Mombo I.M.
      • Nkoghe D.
      • Mboui Ondo S.
      • Jiolle D.
      • et al.
      Zika virus in Gabon (Central Africa)—2007: a new threat from Aedes albopictus?.
      A macular or papular rash (90%), fever (65%), arthritis or arthralgia (65%), non-purulent conjunctivitis (55%), myalgia (48%), headache (45%), and retro-orbital pain (39%) have been the most commonly reported symptoms,
      • Buathong R.
      • Hermann L.
      • Thaisomboonsuk B.
      • Rutvisuttinunt W.
      • Klungthong C.
      • Chinnawirotpisan P.
      • et al.
      Detection of Zika virus infection in Thailand, 2012–2014.
      followed by anorexia, vomiting, diarrhea, stomach aches, dizziness, leg pain, lymphadenopathy, and hypotension. No deaths, hospitalizations, or hemorrhagic manifestations have been documented.
      • Duffy M.R.
      • Chen T.H.
      • Hancock W.T.
      • Powers A.M.
      • Kool J.L.
      • Lanciotti R.S.
      • et al.
      Zika virus outbreak on Yap Island, Federated States of Micronesia.
      • Buathong R.
      • Hermann L.
      • Thaisomboonsuk B.
      • Rutvisuttinunt W.
      • Klungthong C.
      • Chinnawirotpisan P.
      • et al.
      Detection of Zika virus infection in Thailand, 2012–2014.
      In the Indonesian outbreak among humans in 1977–1978, no rash was reported.
      • Olson J.G.
      • Ksiazek T.G.
      • Suhandiman
      • Triwibowo
      Zika virus, a cause of fever in Central Java, Indonesia.
      In Eastern Nigeria, two patients presented jaundice.
      • Macnamara F.N.
      Zika virus: a report on three cases of human infection during an epidemic of jaundice in Nigeria.
      There was early evidence of neurotropism of the virus,
      • Dick G.W.
      • Kitchen S.F.
      • Haddow A.J.
      Zika virus. I. Isolations and serological specificity.
      which spares all body tissue except for nervous tissue.
      • Dick G.W.
      Zika virus. II. Pathogenicity and physical properties.
      Intracerebral inoculation of infected human blood in suckling albino Swiss mice was followed by proliferation of the virus in their nervous tissue.
      • Fagbami A.H.
      Zika virus infections in Nigeria: virological and seroepidemiological investigations in Oyo State.
      ZIKV infection has been associated with Guillain–Barré syndrome (GBS) in Martinique and French Polynesia.
      • Oehler E.
      • Watrin L.
      • Larre P.
      • Leparc-Goffart I.
      • Lastere S.
      • Valour F.
      • et al.
      Zika virus infection complicated by Guillain–Barré syndrome—case report, French Polynesia, December 2013.
      • Roze B.
      • Najioullah F.
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      • Brouste Y.
      • Cesaire R.
      • et al.
      GBS Zika Working Group
      Zika virus detection in urine from patients with Guillain–Barré syndrome on Martinique, January 2016.
      During the ZIKV outbreak in French Polynesia in 2013–2014, the incidence of GBS increased 20-fold,
      • Oehler E.
      • Watrin L.
      • Larre P.
      • Leparc-Goffart I.
      • Lastere S.
      • Valour F.
      • et al.
      Zika virus infection complicated by Guillain–Barré syndrome—case report, French Polynesia, December 2013.
      and a case–control study of a large series of patients confirmed the link between ZIKV infection and GBS. Further, the same study did not find any evidence that past or concurrent dengue infection was a causative or predisposing factor for GBS.
      • Cao-Lormeau V.M.
      • Blake A.
      • Mons S.
      • Lastere S.
      • Roche C.
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      • et al.
      Guillain–Barré syndrome outbreak associated with Zika virus infection in French Polynesia: a case–control study.
      Additionally, microcephaly and various ophthalmological findings and neurological symptoms have been observed in fetuses and infants born to infected mothers.
      • Ventura C.V.
      • Maia M.
      • Ventura B.V.
      • Linden V.V.
      • Araujo E.B.
      • Ramos R.C.
      • et al.
      Ophthalmological findings in infants with microcephaly and presumable intra-uterus Zika virus infection.
      • Petersen E.
      • Wilson M.E.
      • Touch S.
      • McCloskey B.
      • Mwaba P.
      • Bates M.
      • et al.
      Unexpected and rapid spread of Zika virus in the Americas—implications for public health preparedness for mass gatherings at the 2016 Brazil Olympic Games.
      • Mlakar J.
      • Korva M.
      • Tul N.
      • Popovic M.
      • Poljsak-Prijatelj M.
      • Mraz J.
      • Kolenc M.
      • et al.
      Zika virus associated with microcephaly.
      • Rubin E.J.
      • Greene M.F.
      • Baden L.R.
      Zika virus and microcephaly.
      The autopsy findings in the CNS of fetuses were a very small brain, complete absence of the cerebral gyri, severe dilation of both cerebral lateral ventricles, dystrophic calcifications throughout the cerebral cortex, and hypoplasia of the brain stem and spinal cord. Particles consistent with ZIKV were detected on electron microscopy of brain tissue, but not in other tissues.
      • Mlakar J.
      • Korva M.
      • Tul N.
      • Popovic M.
      • Poljsak-Prijatelj M.
      • Mraz J.
      • Kolenc M.
      • et al.
      Zika virus associated with microcephaly.
      • Rubin E.J.
      • Greene M.F.
      • Baden L.R.
      Zika virus and microcephaly.

      6. Diagnosis

      It is challenging to diagnose pregnant women or symptomatic individuals living in or returning from areas endemic for flaviviruses. Flaviviruses trigger the production of cross-reactive antibodies in humans, and they cause dengue, Japanese encephalitis, Saint Louis encephalitis, West Nile fever, yellow fever, and Zika infection, diseases that share some similar symptoms.
      • Roth A.
      • Mercier A.
      • Lepers C.
      • Hoy D.
      • Duituturaga S.
      • Benyon E.
      • et al.
      Concurrent outbreaks of dengue, chikungunya and Zika virus infections—an unprecedented epidemic wave of mosquito-borne viruses in the Pacific 2012–2014.
      • Vorou R.
      Letter to the editor: diagnostic challenges to be considered regarding Zika virus in the context of the presence of the vector Aedes albopictus in Europe.

      Centers for Disease Control and Prevention. Revised diagnostic testing for Zika, chikungunya, and dengue viruses in US public health laboratories. Atlanta: CDC; 2016. Available at: http://wwwcdcgov/zika/pdfs/denvchikvzikv-testing-algorithmpdf.(accessed February 26, 2016).

      The emphasis for diagnostics should be on molecular testing, such as reverse-transcription PCR (RT-PCR), during the first 7 days after symptom onset. After the 7th day, viremia decreases gradually; consequently, a negative RT-PCR does not exclude flavivirus infection, and serological testing should be performed.
      • Buathong R.
      • Hermann L.
      • Thaisomboonsuk B.
      • Rutvisuttinunt W.
      • Klungthong C.
      • Chinnawirotpisan P.
      • et al.
      Detection of Zika virus infection in Thailand, 2012–2014.
      IgM antibodies persist for about 2 to 12 weeks and can be detected by ELISA. If this assay is positive, neutralizing antibody detection assays, e.g., plaque reduction neutralization tests (PRNT), may enable us to identify the virus causing infection.
      • Vorou R.
      Letter to the editor: diagnostic challenges to be considered regarding Zika virus in the context of the presence of the vector Aedes albopictus in Europe.

      Centers for Disease Control and Prevention. Revised diagnostic testing for Zika, chikungunya, and dengue viruses in US public health laboratories. Atlanta: CDC; 2016. Available at: http://wwwcdcgov/zika/pdfs/denvchikvzikv-testing-algorithmpdf.(accessed February 26, 2016).

      Confirmation of the diagnosis of ZIKV infection relies on the detection of ZIKV RNA (RNA extraction) in blood through RT-PCR or pan-flavivirus PCR amplification, followed by sequencing, or virus isolation. Alternatively, a confirmatory diagnosis may be achieved with the co-detection of anti-ZIKV IgM antibodies (ELISA) and a ZIKV PRNT90 (or PRNT80) titer of at least 20, and if West Nile virus or dengue virus needs to be ruled out, a ratio of ZIKV to either dengue virus or West Nile virus PRNT titers of ≥4. In contrast, a probable case of ZIKV infection tests negative by RT-PCR but positive for IgM antibody (ELISA), and has a ZIKV PRNT titer of at least 20, and a ratio of ZIKV to dengue virus or to West Nile virus PRNT titers of <4.
      • Duffy M.R.
      • Chen T.H.
      • Hancock W.T.
      • Powers A.M.
      • Kool J.L.
      • Lanciotti R.S.
      • et al.
      Zika virus outbreak on Yap Island, Federated States of Micronesia.
      • Buathong R.
      • Hermann L.
      • Thaisomboonsuk B.
      • Rutvisuttinunt W.
      • Klungthong C.
      • Chinnawirotpisan P.
      • et al.
      Detection of Zika virus infection in Thailand, 2012–2014.
      • Vorou R.
      Letter to the editor: diagnostic challenges to be considered regarding Zika virus in the context of the presence of the vector Aedes albopictus in Europe.
      • Zammarchi L.
      • Tappe D.
      • Fortuna C.
      • Remoli M.E.
      • Gunther S.
      • Venturi G.
      • et al.
      Zika virus infection in a traveller returning to Europe from Brazil, March 2015.
      The detection of the virus in pooled specimens of mosquitoes is performed with quantitative real-time PCR.
      • Faye O.
      • Faye O.
      • Diallo D.
      • Diallo M.
      • Weidmann M.
      • Sall A.A.
      Quantitative real-time PCR detection of Zika virus and evaluation with field-caught mosquitoes.

      7. Vectors

      The vectors of ZIKV in Africa are distinct from those in South America, Southeast Asia, and the Pacific area. Outside Africa, Aedes aegypti is the principal vector, while Aedes albopictus is also becoming established as a competent vector (Table 2).
      Table 2Mosquitoes in which Zika virus has been detected
      Year of samplingLocationMosquito genus and speciesStudy/assayRef.
      Africa
      1948Zika Forest, UgandaAedes africanusMosquito catches in Zika Forest and first isolation of ZIKV from Aedes africanus pooled specimens
      • Dick G.W.
      • Kitchen S.F.
      • Haddow A.J.
      Zika virus. I. Isolations and serological specificity.
      ,
      • Dick G.W.
      Zika virus. II. Pathogenicity and physical properties.
      1958Zika Forest, UgandaAedes africanusVirus isolation
      • Weinbren M.P.
      • Williams M.C.
      Zika virus: further isolations in the Zika area, and some studies on the strains isolated.
      1964Zika Forest, UgandaAedes africanusVirus isolation
      • Haddow A.J.
      • Williams M.C.
      • Woodall J.P.
      • Simpson D.I.
      • Goma L.K.
      Twelve isolations of Zika virus from Aedes (Stegomyia) africanus (Theobald) taken in and above a Uganda Forest.
      1969Uganda, Bwamba county, Zika ForestAedes africanus, Aedes apicorgenteusVirus isolation from pooled specimens of mosquitoes trapped in Zika Forest
      • McCrae A.W.
      • Kirya B.G.
      Yellow fever and Zika virus epizootics and enzootics in Uganda.
      1976–1980Central African RepublicAedes africanus, Aedes opokRetrospective entomological study with RT-PCR and sequencing
      • Berthet N.
      • Nakoune E.
      • Kamgang B.
      • Selekon B.
      • Descorps-Declere S.
      • Gessain A.
      • Manuguerra J.C.
      • Kazanji M.
      Molecular characterization of three Zika flaviviruses obtained from sylvatic mosquitoes in the Central African Republic.
      1968–2002West Africa: Côte d’Ivoire, Senegal, Burkina Faso, Central Africa RepublicAedes dalzieli, Aedes africanus, Aedes aegypti, Aedes furcifer, Aedes grahamii, Aedes luteocephalus, Aedes vittatus, Aedes opockRetrospective study; phylogenetic analysis, reverse transcription PCR, nucleotide sequencing; numerous recombination events were detected
      • Faye O.
      • Freire C.C.
      • Iamarino A.
      • Faye O.
      • de Oliveira J.V.
      • Diallo M.
      • et al.
      Molecular evolution of Zika virus during its emergence in the 20th century.
      1962–2008SenegalAedes aegypti, Aedes dalzieli, Aedes fowleri, Aedes furcifer (known as Aedes taylori), Aedes luteocephalus, Aedes vittatus, Aedes neoafricanus, Aedes metallicus, Aedes minutus, Anopheles africanus, Anopheles coustani, coustani, Anopheles gambiae s.l., Mansonia uniformis (the higher number of ZIKV isolation events was detected in Aedes furcifer (known as Aedes taylori), Aedes luteocephalus, and Aedes dalzieli)Virus isolation in the mosquito cell line AP61 (Aedes pseudoscutellaris)

      Identification of isolates by immunofluorescence with virus-specific immune ascitic fluid; this was confirmed by complement fixation or neutralization tests
      • Althouse B.M.
      • Hanley K.A.
      • Diallo M.
      • Sall A.A.
      • Ba Y.
      • Faye O.
      • et al.
      Impact of climate and mosquito vector abundance on sylvatic arbovirus circulation dynamics in Senegal.
      2011Southeastern SenegalAedes africanus, Aedes hirsutus, Aedes metallicus, Aedes unilineatus, and Culex perfuscus had the highest infection rates compared to Aedes (Diceronyia) furcifer, Aedes (Fredwardsius) vittatus, Aedes taylori, Aedes luteocephalus, Aedes dalzieli, Aedes aegypti, Mansonia uniformis, and Anopheles coustani, with the lower infection ratesVirus isolation, RT-PCR
      • Diallo D.
      • Sall A.A.
      • Diagne C.T.
      • Faye O.
      • Faye O.
      • Ba Y.
      • et al.
      Zika virus emergence in mosquitoes in southeastern Senegal, 2011.
      2007GabonAedes albopictusRetrospective sero-epidemiological and entomological study in 2014; RT-PCR and sequencing of pooled specimens
      • Grard G.
      • Caron M.
      • Mombo I.M.
      • Nkoghe D.
      • Mboui Ondo S.
      • Jiolle D.
      • et al.
      Zika virus in Gabon (Central Africa)—2007: a new threat from Aedes albopictus?.
      Asia
      1969MalaysiaAedes aegyptiVirus isolation
      • Marchette N.J.
      • Garcia R.
      • Rudnick A.
      Isolation of Zika virus from Aedes aegypti mosquitoes in Malaysia.
      NA; experiment in 2012Singapore(Local in Singapore) Aedes aegyptiInoculation of Ugandan ZIKV in (local in Singapore) Aedes aegypti and subsequent mosquito-borne transmission of the virus
      • Wong P.S.
      • Li M.Z.
      • Chong C.S.
      • Ng L.C.
      • Tan C.H.
      Aedes (Stegomyia) albopictus (Skuse): a potential vector of Zika virus in Singapore.
      NA; experiment in 2014Yap Island, Federated States of Micronesia; human outbreak in 2007Field collected Aedes henselli and Culex quinquefasciatus tested negative for ZIKV; Aedes henselli laboratory infectionExperiment; laboratory infection of Aedes henselli
      • Ledermann J.P.
      • Guillaumot L.
      • Yug L.
      • Saweyog S.C.
      • Tided M.
      • Machieng P.
      • et al.
      Aedes henselli as a potential vector of chikungunya and Zika viruses.
      ZIKV, Zika virus; NA, not applicable.
      In Africa, ZIKV was first isolated from Aedes africanus mosquitoes collected in Zika Forest, Bwamba county, Uganda, in 1948,
      • Dick G.W.
      • Kitchen S.F.
      • Haddow A.J.
      Zika virus. I. Isolations and serological specificity.
      1958,
      • Weinbren M.P.
      • Williams M.C.
      Zika virus: further isolations in the Zika area, and some studies on the strains isolated.
      and 1964.
      • Haddow A.J.
      • Williams M.C.
      • Woodall J.P.
      • Simpson D.I.
      • Goma L.K.
      Twelve isolations of Zika virus from Aedes (Stegomyia) africanus (Theobald) taken in and above a Uganda Forest.
      In 1969, ZIKV was isolated from A. africanus and Aedes apicoergenteus collected in Zika Forest, Uganda.
      • McCrae A.W.
      • Kirya B.G.
      Yellow fever and Zika virus epizootics and enzootics in Uganda.
      In 2014, a retrospective study investigated A. africanus and Aedes opok collected in the Central African Republic, West Africa, from 1976 through 1980. The phylogenetic analysis of this research revealed that the detected ZIKV strains clustered together in the African lineages of ZIKV.
      • Berthet N.
      • Nakoune E.
      • Kamgang B.
      • Selekon B.
      • Descorps-Declere S.
      • Gessain A.
      • Manuguerra J.C.
      • Kazanji M.
      Molecular characterization of three Zika flaviviruses obtained from sylvatic mosquitoes in the Central African Republic.
      Viral isolates from the years 1968 to 2002 in West Africa revealed that ZIKV detected in Aedes dalzieli, A. africanus, A. aegypti, and A. furcifer exhibited many recombination events, which could be attributed principally to the zoophilic mosquito A. dalzieli, which takes blood meals from distinct animal species harboring different ZIKV strains at the same time.
      • Faye O.
      • Freire C.C.
      • Iamarino A.
      • Faye O.
      • de Oliveira J.V.
      • Diallo M.
      • et al.
      Molecular evolution of Zika virus during its emergence in the 20th century.
      Another retrospective study in Senegal, West Africa, investigated samples collected from 1962 through 2008 and detected the ZIKV in Aedes aegypti, Aedes dalzieli, Aedes furcifer (known as A. taylori), Anopheles africanus, Anopheles coustani , Anopheles gambiae s.l., and Mansonia uniformis.
      • Althouse B.M.
      • Hanley K.A.
      • Diallo M.
      • Sall A.A.
      • Ba Y.
      • Faye O.
      • et al.
      Impact of climate and mosquito vector abundance on sylvatic arbovirus circulation dynamics in Senegal.
      In 2011, in southeastern Senegal, ZIKV was isolated from M. uniformis, Culex perfuscus, and Anopheles coustani, but without adequate clarification of their vector competency.
      • Diallo D.
      • Sall A.A.
      • Diagne C.T.
      • Faye O.
      • Faye O.
      • Ba Y.
      • et al.
      Zika virus emergence in mosquitoes in southeastern Senegal, 2011.
      However, in 2007, the first human infection with ZIKV was recognized in Gabon, Central Africa, as a result of the presence of A. albopictus, a species that has invaded the urban areas of the country.
      • Grard G.
      • Caron M.
      • Mombo I.M.
      • Nkoghe D.
      • Mboui Ondo S.
      • Jiolle D.
      • et al.
      Zika virus in Gabon (Central Africa)—2007: a new threat from Aedes albopictus?.
      Until then, the ZIKV epidemic had gone unrecognized as a result of the co-existence with dengue and chikungunya viruses.
      • Grard G.
      • Caron M.
      • Mombo I.M.
      • Nkoghe D.
      • Mboui Ondo S.
      • Jiolle D.
      • et al.
      Zika virus in Gabon (Central Africa)—2007: a new threat from Aedes albopictus?.
      A. albopictus has invaded Cameroon in Central Africa and Mozambique in Southeast Africa, gradually replacing the indigenous A. aegypti,

      Ngoagouni C, Kamgang B, Nakouné E, Paupy C, Kazanji M. Invasion of Aedes albopictus (Diptera: Culicidae) into Central Africa: what consequences for emerging diseases? Parasit Vectors 2015; 8:191.

      and depicts a dynamic expansion in temperate climates across the globe.
      • Kampango A.
      • Abilio A.P.
      The Asian tiger hunts in Maputo city—the first confirmed report of Aedes (Stegomyia) albopictus (Skuse, 1895) in Mozambique.
      In the Pacific, vectors of ZIKV are mosquitoes of the genus Aedes, principally the prevalent A. aegypti, followed by the invading A. albopictus,
      • Calvez E.
      • Guillaumot L.
      • Millet L.
      • Marie J.
      • Bossin H.
      • Rama V.
      • et al.
      Genetic diversity and phylogeny of Aedes aegypti, the main arbovirus vector in the Pacific.
      which are known to transmit chikungunya virus, dengue virus, and ZIKV.
      • Roth A.
      • Mercier A.
      • Lepers C.
      • Hoy D.
      • Duituturaga S.
      • Benyon E.
      • et al.
      Concurrent outbreaks of dengue, chikungunya and Zika virus infections—an unprecedented epidemic wave of mosquito-borne viruses in the Pacific 2012–2014.
      They are considered to be competent vectors of the ZIKV Asian lineage, and their prevalence increased from 2011 to 2014.
      • Roth A.
      • Mercier A.
      • Lepers C.
      • Hoy D.
      • Duituturaga S.
      • Benyon E.
      • et al.
      Concurrent outbreaks of dengue, chikungunya and Zika virus infections—an unprecedented epidemic wave of mosquito-borne viruses in the Pacific 2012–2014.
      ZIKV was isolated from A. aegypti in Malaysia in 1969.
      • Marchette N.J.
      • Garcia R.
      • Rudnick A.
      Isolation of Zika virus from Aedes aegypti mosquitoes in Malaysia.
      In Indonesia in 1978, a human epidemic of ZIKV was presumably propagated by A. aegypti during the rainy season, but no study has been conducted to establish the presence of the virus in mosquitoes.
      • Olson J.G.
      • Ksiazek T.G.
      • Suhandiman
      • Triwibowo
      Zika virus, a cause of fever in Central Java, Indonesia.
      In Singapore, the experimental inoculation of local A. aegypti with the Uganda strain of ZIKV was followed by transmission of the virus.
      • Wong P.S.
      • Li M.Z.
      • Chong C.S.
      • Ng L.C.
      • Tan C.H.
      Aedes (Stegomyia) albopictus (Skuse): a potential vector of Zika virus in Singapore.
      However, on Yap Island, in the Federated States of Micronesia, the most prevalent among the 12 mosquito species belonging to four genera collected was Aedes henselli, and pooled specimens tested negative for ZIKV in two studies; consequently, there is uncertainty about the vector.
      • Duffy M.R.
      • Chen T.H.
      • Hancock W.T.
      • Powers A.M.
      • Kool J.L.
      • Lanciotti R.S.
      • et al.
      Zika virus outbreak on Yap Island, Federated States of Micronesia.
      • Ledermann J.P.
      • Guillaumot L.
      • Yug L.
      • Saweyog S.C.
      • Tided M.
      • Machieng P.
      • et al.
      Aedes henselli as a potential vector of chikungunya and Zika viruses.
      The laboratory inoculation of ZIKV into this mosquito was conducted on Yap Island, with 80% being colonized (when a high inoculum was provided), among which 23% developed infection.
      • Ledermann J.P.
      • Guillaumot L.
      • Yug L.
      • Saweyog S.C.
      • Tided M.
      • Machieng P.
      • et al.
      Aedes henselli as a potential vector of chikungunya and Zika viruses.
      Similarly, in French Polynesia, where an extended epidemic occurred in October 2013, the prevalence of A. henselli is higher than any other species, supposedly rendering it a vector for ZIKV; however, no study has been conducted to detect the virus in pooled specimens,
      • Musso D.
      Zika virus transmission from French Polynesia to Brazil.
      and at the peak of the epidemic, the entomological study pointed at A. aegypti and Aedes polynesiensis.
      • Ioos S.
      • Mallet H.P.
      • Leparc Goffart I.
      • Gauthier V.
      • Cardoso T.
      • Herida M.
      Current Zika virus epidemiology and recent epidemics.
      In Brazil, transmission has been attributed to A. aegypti and A. albopictus. A. aegypti can be found in rural and urban areas transmitting chikungunya virus and four dengue serotypes, but A. albopictus is prevalent in the country.
      • Petersen E.
      • Wilson M.E.
      • Touch S.
      • McCloskey B.
      • Mwaba P.
      • Bates M.
      • et al.
      Unexpected and rapid spread of Zika virus in the Americas—implications for public health preparedness for mass gatherings at the 2016 Brazil Olympic Games.
      • Marcondes C.B.
      • Ximenes M.F.
      Zika virus in Brazil and the danger of infestation by Aedes (Stegomyia) mosquitoes.
      Human travel among several commercial urban areas allows for the rapid movement of vectors (in cars, trucks, planes) along with the infected humans.
      A. albopictus has colonized almost every Mediterranean country and continues to spread through Central and Northern Europe. Aedes japonicus has spread widely in Central Europe, Aedes atropalpus in Northern Italy and the Netherlands, Aedes koreicus on the Swiss–Italian border, Belgium,
      • Boukraa S.
      • Dekoninck W.
      • Versteirt V.
      • Schaffner F.
      • Coosemans M.
      • Haubruge E.
      • Francis F.
      Updated checklist of the mosquitoes (Diptera: Culicidae) of Belgium.
      and Germany, and A. aegypti has established itself on Madeira and around the Black Sea coast (Russia, Abkhazia, Georgia).
      • Schaffner F.
      • Medlock J.M.
      • Van Bortel W.
      Public health significance of invasive mosquitoes in Europe.
      Similar to all arboviruses, ZIKV vectors are influenced by animal population density. Thus, ZIKV could reveal a surprising vector, reservoir, and amplifying host range should it be introduced into novel tropical or temperate natural ecosystems, including Europe.
      • Faye O.
      • Freire C.C.
      • Iamarino A.
      • Faye O.
      • de Oliveira J.V.
      • Diallo M.
      • et al.
      Molecular evolution of Zika virus during its emergence in the 20th century.
      • Kuno G.
      • Chang G.J.
      Biological transmission of arboviruses: reexamination of and new insights into components, mechanisms, and unique traits as well as their evolutionary trends.
      Additionally, vectors such as A. aegypti and A. dalzieli, which feed on several animal species and humans, enhance the transmission rate, as well as concurrent infections and the recombination and reassortment of the genetic material of ZIKV strains.
      • Musso D.
      Zika virus transmission from French Polynesia to Brazil.
      • Kuno G.
      • Chang G.J.
      Biological transmission of arboviruses: reexamination of and new insights into components, mechanisms, and unique traits as well as their evolutionary trends.
      As A. aegypti and A. albopictus thrive in stagnant water collections like those in peri-domestic water supplies used in the absence of piped water provision, proliferation may be encouraged by human population growth or the migratory waves from areas of civil upheaval and the possible subsequent formation of uncontrolled slums. Therefore, consistent public awareness about the significance of eliminating any peri-domestic stagnant water is of critical public health importance.
      • Boukraa S.
      • Dekoninck W.
      • Versteirt V.
      • Schaffner F.
      • Coosemans M.
      • Haubruge E.
      • Francis F.
      Updated checklist of the mosquitoes (Diptera: Culicidae) of Belgium.
      • Erguler K.
      • Smith-Unna S.E.
      • Waldock J.
      • Proestos Y.
      • Christophides G.K.
      • Lelieveld J.
      • Parham P.E.
      Large-scale modelling of the environmentally-driven population dynamics of temperate Aedes albopictus (Skuse).
      • Valerio L.
      • Roure S.
      • Fernandez-Rivas G.
      • Ballesteros A.L.
      • Ruiz J.
      • Moreno N.
      • et al.
      Arboviral infections diagnosed in a European area colonized by Aedes albopictus (2009-2013, Catalonia, Spain).
      • Werner D.
      • Zielke D.E.
      • Kampen H.
      First record of Aedes koreicus (Diptera: Culicidae) in Germany.

      8. Animal hosts

      The virus reservoir was not identified in a 1947 study in Zika Forest, Uganda, where ZIKV was first isolated from rhesus monkeys.
      • Dick G.W.
      • Kitchen S.F.
      • Haddow A.J.
      Zika virus. I. Isolations and serological specificity.
      The monkeys displayed mild or absent clinical presentations, while 5 days after experimental infection, they developed neutralizing antibodies.
      • Dick G.W.
      Zika virus. II. Pathogenicity and physical properties.
      Additionally, anti-ZIKV antibodies were detected in wild mammals in Senegal in 1967–1968.
      • Bres P.
      [Recent data from serological surveys on the prevalence of arbovirus infections in Africa, with special reference to yellow fever].
      In 1969, in Zika Forest, ZIKV was isolated from samples taken from monkeys.
      • McCrae A.W.
      • Kirya B.G.
      Yellow fever and Zika virus epizootics and enzootics in Uganda.
      In Lombok, Indonesia, in 1978, anti-ZIKV antibodies were detected in ducks, goats, cows, horses, bats, and carabaos (water buffalo), but not in chickens, rats, or wild birds, indicating the widespread circulation of the virus in domestic animals.
      • Olson J.G.
      • Ksiazek T.G.
      • Gubler D.J.
      • Lubis S.I.
      • Simanjuntak G.
      • Lee V.H.
      • et al.
      A survey for arboviral antibodies in sera of humans and animals in Lombok, Republic of Indonesia.
      The question of whether birds transfer the virus over long distances remains unanswered.
      • Olson J.G.
      • Ksiazek T.G.
      • Gubler D.J.
      • Lubis S.I.
      • Simanjuntak G.
      • Lee V.H.
      • et al.
      A survey for arboviral antibodies in sera of humans and animals in Lombok, Republic of Indonesia.
      In 1982 in Gabon, antibodies against the virus were again detected in monkeys.
      • Saluzzo J.F.
      • Ivanoff B.
      • Languillat G.
      • Georges A.J.
      [Serological survey for arbovirus antibodies in the human and simian populations of the South-East of Gabon (author's transl)].
      In 1983, antibodies against ZIKV were detected in Pakistan among rodents, domestic sheep, and goats, as well as in human sera.
      • Darwish M.A.
      • Hoogstraal H.
      • Roberts T.J.
      • Ahmed I.P.
      • Omar F.
      A sero-epidemiological survey for certain arboviruses (Togaviridae) in Pakistan.
      Samples collected in 1996–1997 from wild and semi-captive orangutans in Borneo, Malaysia, tested positive for anti-ZIKV antibodies.
      • Wolfe N.D.
      • Kilbourn A.M.
      • Karesh W.B.
      • Rahman H.A.
      • Bosi E.J.
      • Cropp B.C.
      • et al.
      Sylvatic transmission of arboviruses among Bornean orangutans.
      Samples collected from monkeys in West Africa from 1968 through 2002 were examined and the virus detected with RT-PCR,
      • Faye O.
      • Freire C.C.
      • Iamarino A.
      • Faye O.
      • de Oliveira J.V.
      • Diallo M.
      • et al.
      Molecular evolution of Zika virus during its emergence in the 20th century.
      and samples collected between 1962 and 2008 from monkeys in West Africa tested positive for specific ZIKV antigens with serology assays (Table 3).
      • Althouse B.M.
      • Hanley K.A.
      • Diallo M.
      • Sall A.A.
      • Ba Y.
      • Faye O.
      • et al.
      Impact of climate and mosquito vector abundance on sylvatic arbovirus circulation dynamics in Senegal.
      Table 3Animals in which Zika virus was detected
      Year of samplingLocationAnimalAssay virus/antibodyNumber of animals testedPositive animals (%)Ref.
      1947Zika Forest, UgandaRhesus monkeysIntracerebral inoculation into mice and subsequent virus isolationOne rhesus diagnosed with the virus; two others underwent successful experimental inoculation
      • Dick G.W.
      • Kitchen S.F.
      • Haddow A.J.
      Zika virus. I. Isolations and serological specificity.
      ,
      • Dick G.W.
      Zika virus. II. Pathogenicity and physical properties.
      1967–1968

      1962 and 1964
      Senegal 1967–1968

      Ethiopia 1962 and 1964
      Wild mammals, monkeysAntibody detection with HINot reportedWild mammals 2.4%, monkeys 25%
      • Bres P.
      [Recent data from serological surveys on the prevalence of arbovirus infections in Africa, with special reference to yellow fever].
      1969Uganda, Kisubi, Bwamba county, Zika ForestBwamba county monkeys
      Red-tail monkey, black mangabey, and lowland colobus were positive for Zika virus.
      Antibody detection with HI testKisubi red-tail 21

      Bwamba red-tail 52

      Bwamba others 16
      4/21

      23/52

      7/16
      • McCrae A.W.
      • Kirya B.G.
      Yellow fever and Zika virus epizootics and enzootics in Uganda.
      1978Lombok, Indonesia; human outbreak in 1977Ducks, goats, cows, horses, bats, rats, carabaos (water buffalo)HI antibodies (HIA) and detection of antibodies (DA)HIA:

      15 horses

      41 cows

      13 carabaos

      35 goats

      78 chickens

      52 ducks

      71 bats

      25 rats

      17 wild birds

      DA:

      6 horses, 8 cows, 1 carabao, 9 goats, 1 chicken, 2 ducks, 1 bat
      HIA:

      3/15 (20%)

      4/41 (10%)

      1/13 (8%)

      7/35 (20%)

      0/78 (0)

      2/52 (4%)

      6/71 (8%)

      0/25 (0)

      0/17 (0)

      DA:

      All tested negative
      • Olson J.G.
      • Ksiazek T.G.
      • Gubler D.J.
      • Lubis S.I.
      • Simanjuntak G.
      • Lee V.H.
      • et al.
      A survey for arboviral antibodies in sera of humans and animals in Lombok, Republic of Indonesia.
      1982GabonMonkeysAntibody detection with HI/complement fixation test
      • Saluzzo J.F.
      • Ivanoff B.
      • Languillat G.
      • Georges A.J.
      [Serological survey for arbovirus antibodies in the human and simian populations of the South-East of Gabon (author's transl)].
      1983PakistanRodents, domestic sheep and goats (at slaughter), humansAntibody detection157 rodents

      45 cows

      33 buffaloes

      46 sheep

      48 goats
      6/157(3.8%)

      0

      0

      1(2.57%)

      1(2.083%)
      • Darwish M.A.
      • Hoogstraal H.
      • Roberts T.J.
      • Ahmed I.P.
      • Omar F.
      A sero-epidemiological survey for certain arboviruses (Togaviridae) in Pakistan.
      1996–1997Malaysia, BorneoWild orangutans, semi-captive orangutansAntibodies40 wild orangutans, 31 semi-captive orangutans5/40 (13%) wild, 1/31 (3%) semi-captive
      • Wolfe N.D.
      • Kilbourn A.M.
      • Karesh W.B.
      • Rahman H.A.
      • Bosi E.J.
      • Cropp B.C.
      • et al.
      Sylvatic transmission of arboviruses among Bornean orangutans.
      1968–2002West Africa: Côte d’Ivoire and Senegal, Burkina Faso, Central Africa Republic; retrospective study of viral isolatesMonkeysRT-PCR, nucleotide sequencing, recombination detectionNA
      • Faye O.
      • Freire C.C.
      • Iamarino A.
      • Faye O.
      • de Oliveira J.V.
      • Diallo M.
      • et al.
      Molecular evolution of Zika virus during its emergence in the 20th century.
      1962–2008Senegal; retrospective study of viral isolatesMonkey (Erythrocebus patas), Chlorocebus aethiops (also named grivet and African green monkey)Virus isolation in the mosquito cell line AP61 (Aedes pseudoscutellaris); identification of isolates by immunofluorescence with virus-specific immune ascitic fluid and confirmed by complement fixation or neutralization testsNA
      • Althouse B.M.
      • Hanley K.A.
      • Diallo M.
      • Sall A.A.
      • Ba Y.
      • Faye O.
      • et al.
      Impact of climate and mosquito vector abundance on sylvatic arbovirus circulation dynamics in Senegal.
      HI, hemagglutination inhibition; NA, not applicable.
      a Red-tail monkey, black mangabey, and lowland colobus were positive for Zika virus.
      The antibody detection assays run the risk of cross-reaction with other flaviviruses co-circulating with the ZIKV, thus challenging the safe interpretation of published data. Furthermore, early laboratory methods for the detection of antibodies were of uncertain specificity and sensitivity, and antigen and molecular assays had not been developed.

      9. Conclusions

      There are few entomological and vector capacity studies and limited literature regarding the investigation of the prevalence of the virus in wild and domestic animals in temperate and tropical climates. This is probably because the virus has caused mild or no clinical symptoms in humans and animals until recently.
      The dissemination of ZIKV throughout the Pacific and South America after the French Polynesia outbreak of ZIKV in 2013 is not in doubt. There is no information about the possibility of trans-ovarian transmission of the virus in mosquitoes. The virus has been identified in the genera Aedes, Anopheles, and Mansonia only in Africa, and there has been no such pooled specimen examination of these genera in Asia, the Pacific, or the Americas. In the Pacific and Southeast Asia, however, experimental inoculation of A. aegypti and A. henselli was successful.
      A. albopictus has expanded worldwide and can adapt to distinct ecosystems and trigger arboviral outbreaks. A. aegypti, which is prevalent in densely populated areas of South America, is recognized as difficult to eradicate and control.
      • Marcondes C.B.
      • Ximenes M.F.
      Zika virus in Brazil and the danger of infestation by Aedes (Stegomyia) mosquitoes.
      There are concerns about the vast majority of asymptomatic while contagious infections, the recent neurological complications and sequelae in adults and fetuses/newborns,
      • Faye O.
      • Freire C.C.
      • Iamarino A.
      • Faye O.
      • de Oliveira J.V.
      • Diallo M.
      • et al.
      Molecular evolution of Zika virus during its emergence in the 20th century.
      and the potential genetic evolution of this RNA virus, which pose a threat for subsequent novel neurological and other manifestations. This is a vector-borne infection that can be transmitted via sexual intercourse.
      In summary, there is insufficient information regarding the animal reservoirs and amplification hosts, including domestic animals, and the vectors of ZIKV, as well as the vector capacity of the genus Aedes and genus Anopheles. This represents a public health emergency, and it is essential that we improve our understanding of these factors because they will define the transmission dynamics and geographic distribution of ZIKV, as well as indicate the timing and scale of environmental public health interventions.
      Ethical approval: Approval was not required.
      Conflict of interest: None declared.

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