EMERGING INFECTIOUS DISEASES
Volume 1, Number 1, January-March 1995


                           Dispatches

Emergence of Barmah Forest Virus in Western Australia*

To the editor: Barmah Forest (BF) virus is a mosquito-borne
alphavirus, found only in Australia, which causes outbreaks of
polyarthritis in humans. The disease is very similar to epidemic
polyarthritis caused by infection with Ross River virus, another
Australian alphavirus. BF virus was first isolated from
mosquitoes in the State of Western Australia in 1989. After this,
small clusters of human cases were diagnosed in the arid northern
and central regions of Western Australia in 1992, and the first
substantial outbreak of human disease due to infection with BF
virus (BF virus disease) occurred in the southwestern region of
the state during the spring and summer (September-March) of
1993-94 (2). No evidence of BF virus activity had been found in
these regions before these events, which suggests that the virus
had only recently been introduced to Western Australia. This
report describes the timing and distribution of BF virus disease
in humans and the isolation of the virus from mosquitoes in
Western Australia, which corroborate the view that BF virus is an
emerging virus in this state.
_____
*This report is adapted from, and expands on, a previous bulletin
(1).

The ecology of Australian arboviruses that cause human disease,
including BF virus, has recently been reviewed (3). BF virus was
first isolated from Culex annulirostris mosquitoes collected at
the Barmah Forest in northern Victoria (southeastern Australia)
in 1974 (4). It was first shown to infect humans in New South
Wales (central-eastern and southeastern Australia) in 1986 (5)
and was reported as a cause of clinical disease in humans in 1988
(6). The most common clinical features include polyarthritis,
arthralgia, myalgia, fever, rash, and lethargy (7); in some
cases, symptoms may persist for more than 6 months (2). Although
the symptoms are similar to those caused by infection with Ross
River virus, there is little cross-reaction between the two
viruses in serologic tests (8), and differentiating between
infections caused by either is generally not difficult. The first
true outbreak of BF virus disease occurred concurrently with an
outbreak of Ross River virus infection at Nhulunbuy in the
Northern Territory in early 1992 (9).

The principal vectors of BF are believed to be mosquitoes, and
although the vertebrate hosts of BF virus are not known,
serologic surveys in eastern Australia have suggested that
marsupials are involved in the natural cycle.

BF virus was first detected in Western Australia in 1989. Since
then, 73 isolates of the virus have been obtained from mosquitoes
trapped in several different regions of Western Australia (Table
1). The first human cases of BF virus disease in Western
Australia were reported in 1992, and 67 serologically confirmed
cases have now been diagnosed. The locations of towns where human
cases have occurred or where mosquitoes that yielded BF virus
were collected are shown in Figure 1. (Figure cannot be viewed in
ASCII.)


Table 1. Mosquito species from which BF virus was isolated in
Western Australia by region and date, 1989 1993*

Region          Locality     Species            Date     Isolates

East Kimberley  Billiluna  Ae. bancroftianus    22 Apr 1989   1
East Kimberley  Billiluna  Ae. eidsvoldensis    22 Apr 1989   3
East Kimberley  Billiluna  Ae.                  22 Apr 1989   1
                            pseudonormanensis
East Kimberley  Billiluna  An. amictus          22 Apr 1989   2
East Kimberley  Billiluna  An. annulipes s.l.   22 Apr 1989   1
East Kimberley  Halls Creek Cx. annulirostris   11 Feb 1993   1


West Kimberley  Broome     Ae. vigilax       10-16 Feb 1993   9
West Kimberley  Fitzroy    Cx. annulirostris    13 Feb 1993   1
                 Crossing
West Kimberley  Willare    Ae. normanensis      16 Mar 1993   1

Pilbara         Onslow     Ae. EN Marks'      3-14 Jun 1992   3
  (Fortescue)                sp. #85
Pilbara         Onslow     Cx. annulirostris    13 Jun 1992   1
  (Fortescue)
Pilbara         Onslow     An. amictus       13-14 Jun 1992   2
  (Fortescue)
Pilbara         Exmouth     Ae. vigilax  16 Jun-11 Jul 1992   7
  (Fortescue)

        
Gascoyne (West) Minilya     Ae. eidsvoldensis    7 Jul 1992   5
Gascoyne (West) Minilya     Ae. eidsvoldensis    7 Jul 1992   1
                              (bloodfed)
Gascoyne (West)  Minilya    Ae. EN Marks'        7 Jul 1992   1
                              sp. #85
Gascoyne (West)  Carnarvon  Ae. eidsvoldensis   12 Jul 1992   3
Gascoyne (West)  Carnarvon  Ae. EN Marks'       12 Jul 1992   1
                               sp. #85
Gascoyne (West)  Carnarvon  Cx. quinquefasciatus 12 Jul 1992  1
Gascoyne (West)  Carnarvon  Unidentifiable      12 Jul 1992   1
                              mosquitoes

       
Central Coastal  Karnup     Cx. annulirostris     4 Jan 1993  1
Central Coastal  Karnup     Cq. species near      4 Jan 1993  4
                              linealis
Central Coastal  Perth      Cx. annulirostris     6 Jan 1993  1

        
South Coastal    Australind  Ae. camptorhynchus   6 Jul 1993  1
South Coastal    Mandurah    Ae.            5 Aug-5 Oct 1993 10 
                   (Peel)     camptorhynchus
South Coastal    Busselton   Ae.            1 Sep-15 Nov 1993  9
South Coastal    Busselton   Cx. globocoxitus      1 Nov 1993  1

                                                        Total 73
_____
* Numbers of mosquitoes trapped and processed and estimated
minimum field infection rates for each region will be published
in detail elsewhere.
  Refer to Figure 1 for location of regions and towns from which
isolates of BF virus were obtained.


Eight isolates of the virus were obtained from five different
mosquito species (Table 1) collected at Billiluna, a small,
remote aboriginal community in an arid area in the southeastern
Kimberley region in April 1989 (10). The infected mosquitoes were
collected 3 weeks after heavy local rains. Only moderate wet
season rains were recorded in the remainder of the Kimberley
region, and no cases of BF virus disease were reported from any
region in Western Australia that year. There have been no
subsequent isolations of BF virus from mosquitoes collected at
Billiluna, despite annual collections in the region. No human
cases have been reported from Billiluna.

The first cases of BF virus disease in Western Australian were
reported almost 3 years later, either individually or in small
clusters from towns in the arid East Kimberley, Pilbara,
Gascoyne, Murchison and Southeast (Goldfields) regions between
April and September (Autumn-Spring) 1992. Most activity was
reported from the towns of Exmouth (six cases) and Carnarvon
(four cases). All of these cases occurred during or just after
much larger outbreaks of disease caused by Ross River virus. This
suggested that BF and Ross River viruses may have similar
mosquito vectors and require similar environmental conditions for
successful transmission. The main environmental factor
contributing to the 1992 outbreaks of Ross River virus disease
was extremely heavy rain in these normally arid regions during
autumn and winter (11).

BF virus was isolated from five species of mosquito in the
Fortescue region of the Pilbara and from three species in the
West Gascoyne, just prior to, and during, these arid-region
outbreaks. In coastal regions of the Pilbara, the main vector of
BF virus appears to be Aedes vigilax, a salt marsh-breeding
species. Large numbers of this species develop after very high
tides or heavy rains on salt marshes. It is also the main vector
of Ross River virus in these regions (12). Several other
temporary freshwater ground pool-breeding species in the subgenus
Ochlerotatus, particularly Ae. eidsvoldensis and Ae. EN Marks'
species #85, were found to be infected with the virus in inland
areas or coastal areas where such pools develop. These
preliminary investigations also suggested that both BF and Ross
River virus can co-circulate. Both viruses were isolated from
different mosquitoes of the same species collected in the same
trap on several occasions.

A further six cases of BF virus disease were reported after
record wet season rains in the Kimberley region in early 1993.
The cases occurred just after mosquitoes in the Kimberley region
had been collected by personnel from this laboratory. These
collections yielded 12 isolates of BF virus. Eleven of these were
from Ae. vigilax and Cx. annulirostris mosquitoes trapped less
than 2 weeks after the first heavy wet season rains near the West
Kimberley towns of Broome and Fitzroy Crossing and the East
Kimberley town of Halls Creek (see Figure 1 for locations, Table
1 for isolation details). A twelfth isolate was obtained from Ae.
normanensis collected 5 weeks after the first rains at Willare in
the West Kimberley. The timing of the collections was such that
all three mosquito species could have transmitted BF virus to the
infected persons in the region. Vector competence studies are
required to determine if one or more species were likely to have
been the main vectors.

A single case was reported from the metropolitan area of Perth,
the state's capital, in August 1992. This was the first evidence
of BF virus activity in the temperate and populous southwestern
region of Western Australia. However, the travel history of the
patient was not obtained. Then, in early January 1993, this
laboratory isolated BF virus from Cx. annulirostris and
Coquillettidia species near linealis* mosquitoes collected at
Karnup, south of Perth (Table 1). A week later a single human
case was reported from an address near the site at which the
mosquitoes were trapped. BF virus was also isolated from Cx.
annulirostris mosquitoes trapped in the southern suburbs of Perth
in early January 1993, providing evidence that the virus may be
transmitted to humans in the metropolitan area. Two further cases
were reported from the Perth metropolitan area, one in February
and one in May 1993. Again, no travel histories were available
for these patients, but it appears that the virus remained and
was actively transmitted in the southwest during the autumn and
winter of 1993, as it was isolated from Ae. camptorhynchus
mosquitoes trapped in July and August (Table 1).
_____
*This species is similar to, but distinct from, Coquillettidia
linealis, according to E.N. Marks, the leading Culicid taxonomist
in Australia.

A larger outbreak of BF virus disease occurred in the southwest
region between September 1993 and March 1994. This has been
described in detail elsewhere (2). Twenty-eight serologically
confirmed cases were reported from the southwest region during
that period. Of these, more than half (17 cases) were in or near
the small coastal towns of Mandurah (Peel) and Busselton during
spring (September-November) of 1993. BF virus was isolated on 20
occasions from pools of Ae. camptorhynchus mosquitoes collected
in the Mandurah and Busselton regions before and during the
outbreak (Table 1), thereby implicating that species, along with
Cx. annulirostris and Cq. species near linealis, as an important
vector in the southwest. Ae. camptorhynchus breeds in salt
marshes and brackish wetlands during all but the hottest months
of the year in the southwest and is the main vector of Ross River
virus in the region (3, 11). The ratio of the carriage rate of BF
virus in Ae. camptorhynchus during the outbreak to the number of
human cases was very high compared with the rate observed for
Ross River virus in Ae. camptorhynchus in the same regions during
previous Ross River virus outbreaks (M.D. Lindsay, C.A. Johansen,
and J.S. Mackenzie, unpublished observations). This suggests that
the ratio of subclinical (therefore unreported) to clinical cases
may be much larger with BF virus than with Ross River virus or
that fewer humans were infected, possibly because Ae.
camptorhynchus may not transmit BF virus to humans as efficiently
as it does Ross River virus. Seven cases were reported between
November 1993 and March 1994 in small towns in the inland
southwest region in a later cycle of virus activity.
Unfortunately, no collections of mosquitoes were carried out in
the region during that time. Small clusters of cases or
individual cases were also reported from several other regions of
Western Australia during this time, including three additional
cases from Broome in the West Kimberley region, presumably
associated with the 1993-94 wet season.

BF virus disease was made a notifiable disease in Western
Australia in June 1994 as a direct result of the 1993-94
southwest outbreak (Health [Infectious Diseases] Amendment Order
1994, Government Gazette, Western Australia, 24 June 1994). The
outbreak was also the first report of a substantial number of
cases in the absence of Ross River virus activity anywhere in
Australia. Ross River virus is endemic in the Mandurah (Peel)
region but only one case of Ross River virus disease was reported
from the area during spring-summer (September-February) 1993-94.
This is the lowest recorded number of cases for that period in
the region since record keeping began in 1984. Environmental
conditions and vector mosquito populations in the southwest were
unfavorable for Ross River virus transmission during the BF
outbreak. In particular, populations of Ae. camptorhynchus from
October onwards were much smaller than in years when larger
numbers of cases of Ross River virus disease were reported (M.D.
Lindsay, C.A. Johansen, J.S. Mackenzie, unpublished
observations). It is not known whether the BF virus outbreak
occurred because BF virus can circulate under conditions that are
not suitable for Ross River virus activity or whether extremely
low levels of immunity in "virgin" vertebrate host and human
populations in the southwest may have enhanced transmission
cycles.

Surveillance and epidemiologic studies carried out by this
laboratory in the north of Western Australia since 1972 and in
the southwest since 1987 have found no convincing evidence of BF
virus activity in these regions prior to the events described in
this report. No BF virus was isolated from the north of Western
Australia before 1989, despite large-scale processing of
field-caught mosquitoes over a 17-year period that yielded
hundreds of isolates of other arboviruses. Similarly, no BF virus
isolate was obtained from more than 400,000 mosquitoes collected
throughout the southwest between 1987 and 1992 and processed for
virus isolation. Furthermore, an ongoing serosurvey has found no
evidence of infection with BF virus in more than 1,000
individuals of 18 vertebrate species collected in the southwest
before 1992 (C.A. Johansen, unpublished results). This suggests
that the virus responsible for the recent outbreaks was recently
introduced to Western Australia. The means of introduction,
initially to the northwest and more recently to the southwest of
Western Australia, is not known. In view of the activity at
Nhulunbuy in the Northern Territory, before the first Western
Australia cases in 1992, it is possible that the virus may have
been introduced from that region in a viremic human or in
livestock. However, little is known about the duration and height
of viremia in infected humans or other animals, and it is not
known whether person-to-person vector-mediated transmission of
Barmah Forest virus can occur. Our laboratory has begun a study
to investigate the molecular epidemiology of BF virus,
particularly whether the strain of virus responsible for the
Western Australia outbreaks was introduced from Eastern Australia
or was a local, hitherto undetected, strain.

Acknowledgments

The authors thank Tony Wright, (Health Department of Western
Australia) for assistance with collection of mosquitoes, Margaret
Wallace, Rosa Egerton-Warburton, Roger Clifton, and Dora Li for
assistance with laboratory processing of mosquito and virus
samples, and staff in the Virology Section, State Health
Laboratory Service, the Health Department of Western Australia,
for carrying out the serologic testing of human sera. This work
was funded by a grant from the Health Department of Western
Australia.

Michael D.A. Lindsay, Cheryl A. Johansen, Annette K. Broom, David
W. Smith,* and John S. Mackenzie 
Department of Microbiology, The University of Western Australia,
Queen Elizabeth II Medical Centre, Nedlands, WA
*State Health Laboratory Services, Queen Elizabeth II Medical
Centre, Nedlands, WA

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