VECTOR-BORNE AND ZOONOTIC DISEASES

Volume 11, Number 11, 2011

REVIEW
ª Mary Ann Liebert, Inc.
DOI: 10.1089/vbz.2011.0631

Usutu Virus in Africa

Birgit Nikolay,1–3 Mawlouth Diallo,2 Cheikh Saad Bouh Boye,4 and Amadou Alpha Sall1

Abstract

Usutu virus (USUV) was discovered in South Africa in 1959. Since then, it has been reported in several African
countries including Senegal, Central African Republic, Nigeria, Uganda, Burkina Faso, Cote d’Ivoire, and
Morocco. In 2001, USUV has been identified for the first time outside of Africa, namely in Europe, where it
caused a significant mortality among blackbirds in Vienna, Austria. In 2009, the first two human cases of USUV
infection in Europe have been reported in Italy, causing encephalitis in immunocompromised patients. The host
range in Africa includes mainly Culex mosquitoes, birds, and also humans with one benign and one severe case.
Given its role as a potential human pathogen and the similar appearance compared with other emerging
arboviruses, it is essential to investigate the natural history and ecology of USUV in Africa. In this regard, we
review the emergence of USUV in Africa, summarizing data about isolations, host range, and potential vectors,
which should help to improve our understanding of the factors underlying the circulation of USUV in Europe
and Africa.

Key Words: Arbovirus(es)—Flavivirus—Usutu virus—Africa.

Introduction 2008). In La Reunion Island, CHIKV acquired a selective ad-

vantage for the transmission by an alternate mosquito vector.

I n the past two decades, attention has been given to

several emerging arboviruses that have become a threat to
human health following environmental, climatic, and eco-
logical changes. In this regard, the introduction, spread, and
establishment of West Nile virus (WNV) in northern America
from 1999 to 2010 has been very illustrative. Indeed, until
then, WNV had been known to be circulating mostly in Africa
and Europe, affecting mainly humans and horses, but rarely
causing severe symptoms such as neurologic disease or death
(Gubler 2007, Gardner 2009). After its introduction into North
America, the virus rapidly established an enzootic cycle in-
fecting local birds and mosquito species (Reisen and Brault
2007), causing major outbreaks of encephalitis (O’Leary et al.
2004).
Another example of an emerging arboviral disease is Chi-
kungunya virus (CHIKV), which has caused large outbreaks
in the Indian Ocean Islands and India since 2004 (Kariuki
Njenga et al. 2008). Up to 2010, more outbreaks in Indonesia,
La Reunion Island, China, and Madagascar demonstrate its
continuous activity and emphasize its role as an emerging
infectious disease (ProMEDmail 2010). CHIKV originates in
Africa and spread to Asia and India (Sudeep and Parashar
Subsequently, the CHIKV outbreak in Italy in the year 2007
indicates its potential to spread and establish in Europe
(Schuffenecker et al. 2006).
Similarly, Usutu virus (USUV), a virus reported to be cir-
culating only in Africa, emerged in 2001 in Europe, causing a
significant number of deaths in blackbirds (Turdus merula)
(Weissenbock et al. 2002). Even though avian infections were
not reported to be fatal in Africa, USUV has been shown to be
highly pathogenic to several bird species in Austria, such as
the blackbird (T. merula), the great gray owl (Strix nebulosa),
the blue tit (Parus coeruleus), the house sparrow (Passer do-
mesticus) (Weissenbock et al. 2003), the great tit (Parus major),
the nuthatch (Sitta europaea), the robin (Erithacus rubecula), and
the song thrush (Turdus philomeus) (Chvala et al. 2007). The
observed symptoms included hepatosplenomegaly, neuronal
necrosis, and necrotic changes of liver, spleen, and heart
(Chvala et al. 2004). As for WNV in northern America, USUV
overwintered in Austria by adapting to local mosquito species
and established a transmission cycle among local birds and
mosquitoes mainly of the Culex species (Weissenbock et al.
2003, Brugger and Rubel 2009). Despite continuing virus cir-
culation after its occurrence in 2001, a decrease in bird

1
Unité des Arbovirus et Virus de Fièvres Hémorragiques, Institut Pasteur de Dakar, Dakar, Senegal.
2
Unité Entomologie Médicale, Institute Pasteur de Dakar, Senegal.
3
University Vienna, Faculty of Life Sciences, Molecular Biology, Vienna, Austria.
4
Université Cheikh Anta Diop, Faculté Medecine, Pharmacie et d’Odonto-Stomatologie, Dakar, Senegal.

1417
1418
mortality has been recognized, probably resulting from the
establishment of herd immunity in bird hosts. Wild bird
surveillance indicates seroconversion in a broad range of wild
birds in Austria (Meister et al. 2008), suggesting that USUV is
already endemic in mosquito and bird species. In addition,
USUV has been identified as a cause of death of blackbirds (T.
merula) in Hungary (Bakonyi et al. 2007), Switzerland (Stein-
metz et al. 2011), and Italy (Busani et al. 2010), in addition to
the detection of the virus in great gray owls (S. nebulosa) and
boreal owls (Aegolius funeris) in northern Italy (Manarolla
et al. 2009). Further, USUV was isolated from Culex pipiens
mosquitoes in Spain (Busquets et al. 2008) and Italy as well as
from Aedes albopictus mosquitoes in Italy (Tamba et al. 2010).
Serological evidence of its circulation has been reported
among blackbird, carrion crow (Corvus corone), magpie (Pica
pica), and turkey (Meleagris gallopavo) (Buckley et al. 2003) in
the United Kingdom, sentinel chicken in the United Kingdom
(Buckley et al. 2006) and Italy (Lelli et al. 2008), white stork
(Ciconia ciconia), common redstart (Phoenicurus phoenicurus),
and osprey (Pandion haliaetus) in Germany (Linke et al. 2007),
eurasian coot (Fulica atra) in the Czech Republic (Hubalek
et al. 2008), and black-headed gull (Larus ridibundus) in Poland
(Hubalek et al. 2008). Moreover, USUV antibodies were de-
tected in horses in Italy (Lelli et al. 2008).
In September 2009, the first two human USUV infections in
Europe have been reported in Italy, representing the first cases
of human neuroinvasive infection ever, even though neu-
roinvasiveness in mice after experimental infection has been
already demonstrated (Weissenbock et al. 2004). The patients,
an orthotropic liver transplantation recipient and a patient
with diffuse large B-cell lymphoma, suffered from severe
neurological impairment caused by encephalitis, demon-
strating the role of USUV as a human pathogen at least
for immunocompromised individuals (Cavrini et al. 2009,
Pecorari et al. 2009).
Because of the mortality among some bird species after its
introduction into Europe, further attention was given to USUV,
leading to the availability of more information. However, in
Africa, although the virus was identified in the late 1950s, only
very limited data have been published. Given the potential of
further geographic expansion, changes in the host range (in-
cluding humans), and the possible modification of biological
features of USUV in Europe or other regions of the world, we
review in this article the ecology of USUV in Africa to under-
stand more completely the patterns and processes underlying
its emergence and identify the gaps in our knowledge.
Discovery and Description of the Virus
USUV was recovered for the first time in January 1959 from
a female adult mosquito of the Culex neavei species in the area
of Natal, South Africa (McIntosh 1985), a location equivalent
to a tropical coastal lowland and savannah woodland, and
was named after a river in Swaziland (Woodall 1964).
USUV is a flavivirus (Flaviviridae family) belonging to the
Japanese encephalitis serocomplex (De Madrid and Porter-
field 1974, Poidinger et al. 1996). The USUV genome is a
positive-sense, single-stranded RNA genome of 11,064–11,066
nucleotides length (Weissenbock et al. 2002, Bakonyi et al.
2004, 2007) with a type I cap structure and no poly(A) tail
(Hurrelbrink and McMinn 2003). It is organized as a typical
flavivirus with one open-reading frame encoding a 3434-
NIKOLAY ET AL.
amino-acid-residue polyprotein, which is subsequently
cleaved into three structural (core, membrane, and envelope)
and eight nonstructural (NS1, NS2A, NS2B, NS3, NS4A, 2K,
NS4B, and NS5) proteins (Bakonyi et al. 2004).
Phylogenetic analysis of the NS3 and NS5 coding regions as
well as full-length genome nucleotide sequences of the USUV
reference strain from South Africa (AY453412) allowed its
classification within the mosquito-borne cluster of flavi-
viruses, close to Murray Valley Encephalitis virus and Japa-
nese Encephalitis virus (Fig. 1) (Kuno et al. 1998, Cook and
Holmes 2006). At present, when comparing the three USUV
full-length genome nucleotide sequences from South Africa
(AY453412), Vienna (AY453411), and Budapest (EF206350),
they exhibit 97%–99.9% and 99% homology for nucleotides
and amino acids, respectively (Bakonyi et al. 2004, 2007).
Further, the partial sequences of the E protein coding region of
12 strains isolated in Austria show 95.9%–96.2% nucleotide
identity and 98.9%–99.1% amino acid identity to the reference
strain (Chvala et al. 2007).
Although no sequence data from USUV isolates from Africa
besides South Africa are available, one subtype isolated from
Culex perfuscus was serologically identified in the Central Af-
rican Republic in April 1969 (Institut Pasteur de Bangui 1969).
A year earlier and the following years, another subtype was
reported in Yaounde (Cameroun), but it was later recognized
as a different viral species named Yaounde virus in the light of
further serological characterization (CDC 1985, CRORA 2005).
The biological characteristics of USUV have been analyzed
by demonstrating its infectivity for several continuous and
primary cell lines derived from various animal species and
human [i.e., Vero, ED, MDBK, PK-15, RK-13, MDCK, DK, CR,
BHK-21, BF, C6, TH1, EqK, GEF, LLC-MK2, HeLa (Bakonyi
et al. 2005), and PS (De Madrid and Porterfield 1969, Stim and
Henderson 1969)].
Geographical Distribution
After its first isolation in South Africa, USUV was isolated in
Senegal, Central African Republic, Burkina Faso, Cote d’Ivoire,
Nigeria, and Uganda (CRORA 2005) [Institut Pasteur de Bangui
(Digoutte 1969), CRORA (Robin 1975, Digoutte 1995, 1998)] and
USUV antibodies have been detected in wild birds in Morocco
(Figuerola et al. 2009). USUV was reported in several European
countries as listed earlier (Fig. 2). It is striking that USUV has
been isolated only in African countries in which entomological
surveillance programs have been undertaken, suggesting that
its geographic distribution may be much wider than the re-
ported circulation. Therefore, it would be reasonable to inves-
tigate further USUV circulation in other African countries.
In Senegal, where a continuous entomological surveillance
program of the Institut Pasteur de Dakar started in 1972,
USUV has been repeatedly isolated, providing information at
the country level in Africa. The first USUV isolation occurred
in June 1974 in Kedougou, followed by further isolations in
November/December 1993 in the area of Barkedji and in
July 1998 again in Kedougou (Fig. 3) [CRORA (Robin 1975,
Digoutte 1995, 1998)]. Until 2003, only seven strains had been
isolated with minimum infection rates (i.e., number of USUV
isolates/number of mosquitoes per species collected) of
0.06%–1.35%, and therefore, the low level of circulation of
USUV attracted only little attention. A sudden increase
of USUV isolations was noticed in the year 2003, as 141 strains
USUTU VIRUS IN AFRICA 1419

FIG. 1. Localization of Usutu virus (USUV) within the mosquito-borne cluster of the flaviviruses. The analysis of the NS5
gene allowed the localization of USUV close to Japanese encephalitis virus ( JEV) and Murray Valley encephalitis virus
(MVEV), together with Cacipacore virus (CPCV), Yaounde virus (YAOV), Koutango virus (KOUV), Kunjin virus (KUNV),
West Nile virus (WNV), and Alfuy virus (ALFV) (with permission from Cook and Holmes 2006).

were isolated from Cx. neavei species in the area of Barkedji bird species (Table 1) (CDC 1985, CRORA 2005, CRORA,
between October and December, with a higher minimum in- unpublished data).
fection rate of 2.31% (CRORA, unpublished data). In Senegal,
USUV has been mainly isolated from Cx. neavei but also from Mosquitoes
Cx. perfuscus and Aedes minutus mosquitoes. Isolations were
Mosquitoes of the genus Culex are found in all zoogeo-
restricted to the rainy season (CRORA 2005) (CRORA, un-
graphic regions. Several species are involved in transmitting
published data). The reason for the higher isolation number in
Japanese encephalitis in Orient, encephalitis viruses in North
2003 remains unclear, but it is noteworthy that, at the same
America, and also Murray Valley Encephalitis virus and Ross
period, USUV was isolated in the Cote d’Ivoire, Burkina Faso,
River virus in Australia. Culex mosquitoes are known as
and some countries in Europe, suggesting a circulation at the
vectors for arboviruses such as WNV, which is transmitted by
regional level with potential interaction with Europe. Phylo-
three closely related species: Cx. univittatus, Cx. neavei, and Cx.
genetic analysis of isolates in Senegal and other regions where
perexiguus. Given the close morphological characteristics be-
USUV circulation has been reported should shed light on this
tween Cx. univittatus and Cx. neavei, many reported isolations
question.
of USUV from Cx. univittatus might also actually be from Cx.
neavei and vice versa ( Jupp 1971). In general, mosquitoes of
Host Range of USUV in Africa
the Culex genus are considered as ground pool breeders, but
USUV has been mainly isolated from mosquitoes of the larvae have been also found in leaf axils, tree-holes, and crab
Culex species, twice from human serum, and four times from holes. The genus contains mostly ornithophilic species
1420
FIG. 2. Geographical distribution of USUV. USUV has been
detected in Europe, namely in Austria, Hungary, Switzer-
land, Italy, and Spain. Additionally, serological evidence of
USUV circulation has been reported in Germany, the United
Kingdom, Czech Republic, and Poland. USUV has been
isolated in several African countries, such as South Africa,
Senegal, Cote d’Ivoire, Burkina Faso, Nigeria, the Central
African Republic, and Uganda. Further, seroprevalence in
wild bird populations has been reported in Morocco (Weis-
senbock et al. 2002, Buckley et al. 2003, Bakonyi et al. 2007,
Linke et al. 2007, Busquets et al. 2008, Hubalek et al. 2008a, b,
Lelli et al. 2008, Figuerola et al. 2009, Pecorari et al. 2009,
Steinmetz et al. 2011) (CRORA 2005).
(Clements 1999); however, many species have been reported
to have a large host range and feed not only on birds but also
on amphibians, reptiles, humans, and other mammals
(Chandler et al. 1975, 1976, Ba et al. 2006) (Walter Reed Bio-
systematics Unit 2010). Culex females usually bite at night and
FIG. 3. USUV isolations in Senegal. In Senegal, USUV isolation has been reported from two areas, Kedougou and Barkedji.
USUV has been isolated for the first time in Senegal in the year 1974, followed by two isolations in 1993, and four isolations in
1998. In the year 2003, a total number of 141 isolations have been reported [CRORA (Robin 1975, Digoutte 1995, 1998,
CRORA, unpublished data)].
NIKOLAY ET AL.
prefer the canopy (Lundström 1996, Anderson et al. 2004)
where, in accordance with their roost and nest behavior, a
high abundance of birds is observed. Experimental infection
of Cx. neavei with USUV demonstrated that 2 of 10 mosquitoes
were found positive at 14 days postoral infection, although
the virus transmission to hamsters failed (McIntosh 1985).
Additionally, a few isolations were reported from the mos-
quito species Cx. perfuscus and Cx. quinquefasciatus. Regarding
its bionomic and ecology, the latter might be of great interest
in the USUV transmission cycle. Cx. quinquefasciatus belongs
to the Cx. pipiens complex, which has been shown to be in-
volved in USUV epidemic transmission in Europe (Brugger
and Rubel 2009). In addition, Cx. quinquefasciatus is the most
present in the domestic environment and the most anthro-
pophilic among the known USUV vectors. Further, the species
has a population dynamic not related to rainfall, colonizing
artificial habitats such as polluted water in artificial containers
or edifices as ditches, catches, and basins, because of its steady
presence in domestic environment. USUV isolations have
been also reported from mosquito species of the genus Aedes,
Mansonia, and Coquillettidia (CRORA 2005) (Williams et al.
1964). Like Culex mosquitoes, Coquillettidia mosquitoes are
mainly bird-biting species, whereas Mansonia africana, which
is confined to Africa, is mainly attracted to mammals and
humans (Walter Reed Biosystematics Unit 2010).
Considering the bionomics of different mosquito species
and their association with USUV in nature, Cx. neavei may
play a key role in the enzootic transmission of USUV in Se-
negal, whereas species such as Cx. quinquefasciatus may rep-
resent a bridge or an epizootic–epidemic vector.
Human
So far, in Africa, only two isolations of USUV from human
serum have been reported, with very limited information and
clinical description. The first case occurred in 1981 in the
Central African Republic and was a patient with fever and
rash (Institut Pasteur de Dakar 1982–1984), and the second
case was a 10-year-old patient with fever and jaundice iden-
tified in Burkina Faso in 2004 (CRORA, unpublished data).
These cases show that USUV can infect humans and play a
role as a human pathogen, occurring with benign infection
USUTU VIRUS IN AFRICA 1421

Table 1. Geographical Distribution and Host Range of Usutu Virus

Place of isolation Year of isolation Host Number of strains Reference

Burkina Faso 2004 Human 1 CRORA (unpublished data)

Ivory Coast 2004 Culex quinquefasciatus 1 CRORA (unpublished data)
Nigeria 1972 Andropadus virens 1 CRORA (2005)
Bycanistes sharpii 2 CRORA (2005)
Turdus libonyanus 1 CRORA (2005)
Central African Republic 1969 Culex perfuscus 1 Digoutte (1982–1984)
1980 Cx. perfuscus 1 Digoutte (1982–1984)
Mansonia africana 1 Digoutte (1982–1984)
1981 Human 1 Digoutte (1982–1984)
Senegal 1974 Cx. perfuscus 1 CRORA (Robin 1975)
1993 Cx. gr. univitattus 2 CRORA (Digoutte 1995)
1998 Aedes minutus 2 CRORA (Digoutte 1998)
Cx. perfuscus 2 CRORA (Digoutte 1998)
2003 Culex neavei 141 CRORA (unpublished data)
South Africa 1959 Cx. neavei 1 McIntosh (1985)
Uganda 1962 Coquillettidia azurites 1 Williams et al. (1964)
1968 Cx. spp. 1 Henderson et al. (1972)

symptoms such as fever and rash but also jaundice. As ex-
emplified by WNV or CHIKV, more virulent strains can
emerge and constitute a serious threat to human health, as the
observed USUV neuroinvasiveness in an immunocompro-
mised patient in Italy (Pecorari et al. 2009). However, the
number of cases of human USUV infections is rather limited
and more clinical work on infected patients is necessary to
define its pathogenicity for humans.
Rodents
The isolation of USUV has been described from a rodent
species (Praomys) in the Central African Republic, but it
turned out to be the serologic variant S-t Y 276, which was
later named Yaounde virus. Even though no isolation from
mammals has been reported, guinea pigs and newborn and
weaning mice have been shown to be sensitive to intracerebral
inoculation with USUV (CDC 1985). A rodent species (Arvi-
canthis abyssinicus) showed a trace of viremia after in-
traperitonial inoculation (Simpson and Lule 1964). However,
the available information is not enough to draw a conclusion
about rodents serving as hosts for USUV, suggesting that
fieldwork is needed to identify potential rodent hosts.
Birds
USUV has been isolated from the bird species piping
hornbill (Bycanistes sharpei), little greenbull (Andropadus
virens), and Kurrichane thrush (Turdus libonyanus) in Nigeria
in 1972 (CDC 1985). Additionally, antibodies against USUV
were detected in a blackbird (T. merula) in Morocco (Figuerola
et al. 2009). This is consistent with the fact that many mos-
quitoes of the Culex subgenus are ornithophilic and allows
first speculations about USUV transmission cycles. However,
all mentioned birds are not migratory species, suggesting that
they are probably not involved in dispersing the virus to
Europe. In 2005, serological studies demonstrated the pres-
ence of USUV antibodies in numerous migratory wild birds in
Austria, such as the kestrel (Falco tinnunculus), the reed war-
bler (Acrocephalus scirpaceus), the marsh harrier (Circus aeru-
ginosus), the barn-swallow (Hirundo rustica), the lesser
whitethroat (Sylvia curruca), the whitethroat (Sylvia commu-
nis), the garden warbler (Sylvia borin), the house martin (De-
lichon urbica), and the pied flycatcher (Ficedula hypoleuca)
(Meister et al. 2008). These species might be candidates for the
introduction of USUV into Europe but remain to be further
investigated.
Prospects for Future Research in Africa
Besides several reported isolations, there are very limited
data available about the host range, phylogeny, and ecology
of USUV in Africa. Given its origin in that continent, it is
essential to gain a better knowledge about this area to un-
derstand the evolution of USUV and its emergence in Europe.
The first cases of human infections, already demonstrating its
potential severity as a human pathogen, occurred in Africa
before the first European cases in 2009 in Italy (Cavrini et al.
2009, Pecorari et al. 2009). The similarities of its pattern with
the WNV scenario, the neuroinvasiveness in immunocom-
promised patients, as well as its experimental neuropatho-
genicity in mice (Weissenbock et al. 2004) emphasize the need
to be cautious about its potential threat to human health.
Many arboviral infections have been observed to either be
asymptomatic or occur with an influenza-like illness. Never-
theless, the mosquito-borne flaviviruses also contain impor-
tant human pathogens that cause central nervous system
disease, coma, or death. In this light, there is an urgent need to
understand the underlying mechanisms of flaviviruses
emergence, and USUV might be a useful model as it emerged
in several European countries within a limited time period
and was able to adapt to new hosts and environments
(Weissenbock et al. 2002, Buckley et al. 2003, 2006, Bakonyi
et al. 2007, Lelli et al. 2008). Reported infections of humans
indicate a role of USUV as human pathogen; however, more
clinical research is needed to estimate the risk for human
health. The investigation for the seroconversion for USUV in
human populations living in concerned areas might give a
better idea about its burden as a human pathogen. However,
as the observed symptoms of human USUV infections are not
very specific, it will also be meaningful to develop better
1422
diagnostic tools taking into account USUV variability in
Africa and enabling an easier detection of USUV infections,
such as the recently developed RT-PCR assay for the identi-
fication of USUV in human plasma, serum, and cerebrospinal
fluid (Cavrini et al. 2011).
To date, transmission cycles of USUV in Africa are unclear,
as the available information about the primary vectors, ver-
tebrate hosts, and the ecology of the virus are very scarce. The
recent observations of USUV in Africa demonstrate that the
virus is isolated mainly from Culex mosquitoes (CRORA
2005), but the vector competence of the different mosquito
species found infected needs to be investigated and combined
with their feeding habits to identify potential vertebrate hosts
for USUV, to gain further insight into its transmission cycle in
nature.
As mentioned earlier, USUV has been isolated from non-
migratory birds in Africa. However, seroprevalence studies in
Europe (Meister et al. 2008) identified several bird species
possibly involved in virus dispersal, but it has to be confirmed
by investigating bird populations in areas where USUV has
been isolated in Africa.
Additionally, the phylogenetic analysis of USUV strains
might help to understand the dispersal of the virus within
Africa and Europe and to gain insight into the interactions be-
tween these two areas. At present, only three full-genome se-
quences of USUV strains are available: the reference strain from
South Africa (AY453412) as well as the strains that emerged in
Austria (AY453411) and Hungary (EF206350). Therefore, fur-
ther sequence analysis of isolates from Africa is needed.
In conclusion, to understand the full range of virus char-
acteristics and factors of emergence, it is necessary to not only
follow the development of its emergence in Europe but also
understand the relationship to the original strains that have
been circulating in Africa for a longer period. Any information
obtained about their characteristics, transmission dynamics,
and impact on host ecology would be a valuable asset to
understand the transmission dynamics in Europe, the dis-
persal, and ways of adaptation of USUV.
Acknowledgments
B. Nikolay is awardee of a scholarship by the Austrian
Federal Ministry for Science and Research (BMWF). The au-
thors thank the two anonymous reviewers for their comments
that helped to improve the paper.
Disclosure Statement
No competing financial interests exist.
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Address correspondence to:
Amadou Alpha Sall
Unité des Arbovirus et Virus de Fièvres Hémorragiques
Institut Pasteur de Dakar
BP 220 Dakar
Senegal
E-mail: asall@pasteur.sn