DTIC ADA260191: Arbovirus Isolations from Mosquitoes Collected During 1988 in the Senegal River Basin

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LA1NR~lScott W. Gordon, RaLph F. TammarieLLo, Kernneth
j.1.inthicum, et aL.
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13. AAS IILAC T (A JaMIT JOO-O r=
SA.jguS: an Septente- 1986, .cc' .ec-ec--aau(.t rnosoLit:es -cT'- .Zcctions
r' the Senega. Ri,ýer basr' to search fý)r ev~aen~e sf Ri4t Va, 'ey Teve, Mrl vir~l,
activity one year after tne '987 outbreak, which occurreo aLona tie SenegaL-Mauritj
ina oorder.More tnan 62,000 soecinens representing 18 species i. seven genera were
COL te cted wit-I carcz.n dioxive-ca~ted, soLid-stete Army fminiatLJ-e Light traps ano
sheep-osited t-aoS. Twenty ý.Arjs 7soatians 'ram CuLex.,Aedes, arcd AmooteLes ms,7e
were recovered 1'rom six Locations: Fanaye DieryC11),8cde~foujr),Natam(two),Diongi..
(one;,NdiaLeme(one), and Ngoui~orle3.Species yieLding viraL' isc.ares were Anopheles
orar~eensis Ceight&.CLutex tra-irycistre.xuiittsg-(ht)C~,tna~
Ctwo) ,Cx~poiciLLioes(two),Ae.hirsut.us~one),and An.gambiae(ene). Vir~jses were icldentjific
by cot'otement fixatior, ano virus ano F.o.aque-reduction neutraltizaticni testing as
Ngari(Bunyavir'..s, Bunyav~ridae) (n=15),Babanki(A~phavirus.Togav''idae)(n)=3).Bagaza
(FL avivi rjs~rLav-,i ridae)Cnz.) ard Bangui (8unyavi rus-L ink)(n=1 ) No evicfente of ar->
RVF virai. activity in the SenegaL. River Basin was dotected ir the mosquitoes Testeo
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VIRUS, ARBOVIRUSES,'RIFT,.VALLEY FEVER 1. P.C Cora -
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Ir- JI rop. Med tlvg.. 47(6). 11)12, pp 742-748
(opyright ! 1c 92 h) The American Soc(cid:127)'c of Tropical Medicinc and Higiene
ARBOVIRUS ISOLATIONS FROM MOSQUITOES COLLECTED
DURING 1988 IN THE SENEGAL RIVER BASIN
SCOTT W. GORDON, RALPH F. TAMMARIELLO. KENNETH J. LINTHICUM.
DAVID J. DOHM, J. P. DIGOUTTE. AND M. A. CALVO-WILSON
Departmyent of.4rhoviral Entomology. Virology Division. L'.S. .Irm" Medical Research Instiute
of lntctious Diseases. Fort Detrwk, Frederick. .arviand: Institut Pasteurd e Dakar. Dakar,
Senegal
Abstract. During August and September 1988, we collected adult mosquitoes from 14
locations in the Senegal River basin to search for evidence of Rift Valley fever (RVF) viral
activity one year after the 1987 outbreak, which occurred along the Senegal-Mauritania
border. More than 62,000 specimens representing 18 species in seven genera were collected
with carbon dioxide-baited, solid-state Army miniature light traps and sheep-baited traps.
Twenty virus isolations from Culex. .Aedes. and .4nopheles mosquitoes were recovered from
six locations: Fanaye Diery (11). Bode (four), Matam (two), Diongui (one). Ndialene (one).
and Ngoui (one). Species yielding viral isolates were Anopheles pharoensis (eight), Culeh
tritaeniorhynchus( three). Cy. univitattus gr. (three), Cx. antennatus (two), Cx. poicillipes
(two), Ae. hirsutus (one), and .Aln. gambiae (one). Viruses were identified by complement
fixation, and virus and plaque-reduction neutralization testing as Ngari (Buntavirus, Bun-
yaviridae) (n = 15). Babanki (.-1phavirus, Togaviridae) (n = 3), Bagaza (Flav ivirus, Flavi-
viridae) (n = 1). and Bangui (Bunyavirus-like) (n = 1). No evidence of any RVF viral
activity in the Senegal River Basin was detected in the mosquitoes tested.
A major epizootic of Rift Valley fever (RVF) in the Senegal River basin during that rainy sea--
occurred in October-December 1987 in the Sen- son.
egal River basin, centered around the town of
Rosso on the Senegal-Mauritania border (Figure MATERIALS AND METHODS
1).' Cases of human febrile illness and often fatal
hemorrhagic disease were first noted by French Study' area
physicians at the Rosso hospital. In all. 385 lab-
oratory-confirmed human infections ofRVF were Mosquitoes tested in this study were collected
reported by the Institut Pasteur in Dakar, Sen- at 14 locations in the Senegal River Basin (Figure
egal. and estimates of total human involvement 1). The vegetative pattern in the Senegal River
exceeded 1.000 cases.' 'Local domestic animals, basin can be categorized as Sahelian to Sudano-
primarily sheep and goats, were also heavily in- Sahelian savannah, dominated by annual grasses
volved in the outbreak. Serosurveys ofdomestic and widely dispersed trees. particularly Acacia
animals in the Rosso area revealed IgM antibody spp. and Combretacae spp6. Rainfall occurs pri-
to RVF virus in 80% of the domestic animals marily from July through October and ranges
tested.' from 200 mm to 600 mm annually. A water
The magnitude of this outbreak and its ap- development program, instituted by the govern-
parent linkage to the development of a multi- ments of Senegal, Mauritania, and Mali, was re-
national irrigation project' generated intense in- cently established in this area to make better use
terest in conducting studies during the rainy of the Senegal River basin for agricultural pur-
season of 1988 (August-September) to assess the poses. Two dams were constructed on the Sen-
potential for continuing RVF viral activity in the egal River, one at Diama in the delta region,
Senegal River basin. This study describes at- preventing saltwater incursion upstream, and a
tempts to isolate virus from mosquitoes collected second at Manantali in Mali, creating a reservoir
93-02100 742
ARBOVIRUS ISOLATIONS FROM MOSQUITOES IN SENEGAL 743
MAURITANIA
Rso --- Collection Sites
OSSO . 200 km 1. Dakar Bango
2 5 Podor 6 7 2. Ndialene
4 7 " .3. Rhor
St. Louis /1 /(cid:127)8 " ,- 4. Sends
St. (cid:127) 10 us85. Fanaye Diary
10er 6. Ndtoum
13 12 T7B ode
'4pLlnguere 8. Diongui
9. Ngoui
10. Fete Diabe
Dak.r SENEGAL Vallee doMb1oun- 1121.. MYoantaomfere
13. Oahra
Kb(cid:127)Olack ...... .... S or1 14. Tatki
FIGURE 1. %ap of the 14 mosquito collection sites at villages in Senegal. Rivers are indicated by italicized
letters.
to maintain a constant level in the river and en- Iirus isolation
courage the development ofirrigation agriculture
in the region. Mosquito pools were triturated in glass tissue
grinders containing 3.0 ml ofdiluent as described
.Mosquitoc ollct'Lton and identification by Turell and Bailey.' The homogenized sus-
pensions were centrifuged at 800 x g for 20 min
Mosquitoes were sampled from 14 villages and the supernatant was immediately inoculated
during August and September 1988 in sheep- onto two plates of Vero cell monolayers (grown
baited traps and in solid-state Army miniature in 12-well plastic plates). After adsorption for I
light traps (John W. Hock. Co., Gainesville, FL) hr at 35"C, the cells were overlayed with 2 ml
baited with 0.5 kg of dry ice. Collections were well of an agarose-nutrient suspension contain-
frozen in liquid nitrogen in the field and stored ing 0.5% (w/v) agarose in Eagle's basal medium
at - 70"C upon return to the U.S. Army Medical with Earle's salts (plate 1) and a liquid mainte-
Research Institute of Infectious Diseases nance medium consisting of medium 199 with
(USAMRIID). Mosquitoes were identified to Earle's salts, supplemented with 10% fetal bo-
species by using available identification keys,,"(cid:127)' vine serum (plate 2). Cell cultures were then in-
sorted to sex and blood-feeding status. and pooled cubated at 35"C in a humidified atmosphere of
on a refrigerated (4"C) table. Specimens were 5% CO.. Liquid cultures were observed daily for
stored at -70"C until processed for virus isola- cellular cytopathic effects (CPE) for 6-7 days.
tion. Identifications of specimens used as vouch- while agarose-overlayed cells were stained on day
ers for specimens that were assayed were verified 5 by applying a second agarose overlay (I ml/
by the Walter Reed Biosystematics Unit. Smith- well) containing neutral red (330 Ag/ml). Aga-
sonian Institution (Washington, DC). rose-overlayed cells were incubated at 35*C for
744 GORDON AND OTHERS
one additional day, and were then observed for formed in 96-well microtiter plates." A comple-
the presence of plaques. ment-control titration was included in each assay
to detect any anticomplementary activity in the
.......:.n... .. r , ¢,,(cid:127),,t.. immune sera or the viral antigen preparations.
Cell culture seed stocks were prepared for each Plaquer eduction and virus neutralizationt ests in
positive mosquito pool by inoculation (0.2 ml ice
undiluted) of either a plaque-picked suspension
or cell culture supernatant from the original iso- The plaque-reduction neutralization test
lation assay onto fresh Vero cell monolayers (PRNT) was performed in the same manner as
grown in 25-cm2 (T-25) plastic flasks. Viral titers the plaque assay for infectious virus, except that
for each seed stock were determined by plaque a known concentration of virus (50-100 PFLJ)
assay in Vero cells, and expressed as log,, plaque- of each viral strain was incubated at 37"C for 30
forming units (PFU) per ml. Isolates were iden- min with various dilutions of either National
tified at the laboratories of both the USAMRIID Institutes of Health (NIH: Bethesda. MD) ar-
and the Centre CollaborateurOrganization Mon- bovirus reference reagents or type-specific im-
dial del laSuddeReferenceetdeRechcrchepour mune sera before inoculation onto Vero cell
les Arbovirus. Dakar. Senegal. monolayers.' An immune serum was consid-
ered to react positively with a viral strain when
Plreparatione )(immune sera it inhibited ->5 0% of the virus dose. When an-
tisera to some viruses were not available at the
Mouse immuneascilic fluids were prepared for USAMRIID, virus neutralization tests in mice.
a selected number of the viral strains isolated by instead ofPRNT, were conducted at the Institute
using a modification of the method described by Pasteur in Dakar. Senegal. Virus neutralization
Brandt andothers.I'A l:100dilutionofeachcell tests were performed in three-day-old mice in-
culture seed stock was inoculated intracerebrally oculated intracerebrally with 0.02 ml of an in-
into litters of 1-3-day-old suckling mice (ICR cubated mixture of test serum (1:4 dilution) and
strain: 0.03 ml mouse) to provide infected mouse virus (serial 10-fold dilutions) according to the
brains to immunize a group of mice for produc- methods of Causey and others.'
tion of immune ascitic fluid. After the ascitic
fluid was harvested, it was treated to eliminate RESULTS
clot formation. - tescribed by Chiewsilp and
McCown."' Five milliliter aliquots of immune A total of 62,055 mosquitoes representing 18
serum were stored at - 20°C. Normal mouse brain species and seven genera was collected. Cule.\
extract was used to prepare normal ascitic fluid. (eight species, 92.7%). Anopheles (four species.
3.8%). and .4edes (four species. 2.6%) accounted
C ,.,,,,h.,,,aet i /CF) test for more than 99% ofall specimens. Twenty viral
isolates were recovered from 2,793 pools ofunfed
Preparation of antigens. Crude complement- female mosquitoes (Table 1). All 20 isolates pro-
fixing antigens were prepared for each viral iso- duced visible plaques in Vero cells by day 6 post-
late as 10% (w v) infected suckling mouse brain inoculation, while 19 of20 strainsexhibited viral
susvensions in Tris-buffered saline. pH 9.0 or CPE in liquid-overlayed cells. Passage of either
inlected Vero cell culture supernatant fluid.' infected cell culture supernatant or plaque-picked
Normal mouse brain and uninfected Vero cell material of each isolate resulted in characteristic
supernatant control antigens were prepared sim- viral CPE within 4-7 days postinoculation. At-
ilarly. tempts to reisolate virus from the original mos-
The CF test was used to rapidly screen and quito pools were successful in both cell culture
tentatively idcntify the viral isolates. Serial four- systems used.
fold or ten-fold dilutions (starting at 1:4) of an-
t igens were tested against various dilutions (two- Virus identification
fnld siartin2 at 1:8) ofhomologous hyperimmune
sera and a battery of type-specific heterologous Plaque-reduction neutralization test. Prelimi-
hyperimmune sera in a cross-block titration per- nary screening of the viral isolates was performed
ARBOVIRI'S ISOLATIONS FROM MOSQUITOES IN SENEGAL 745
TABLE I
.Ifosquitoes teotd for virus isolation
Species No. tested Virus iolations* MFIRt
htrsutus 1,046 1 Ngari 1:1,046
irrltans 24 0
ocihraceus 88 0
sudancn.vs 480 0
spp. 3 0
.Iti|'dopnia afnutcianus 26 0
In ophe'le
vambiac complex 316 1 Ngari 1:316
pfiaroensis 1.906 7 Ngari 1:272
I Bangui I : 1,906
rulipe' 66 0
ZW'1!iOlMIl 89 0
spp. 10 0
( "u/tv
antennatvu. 21.209 2 Ngari 1:10.604
ta,'ttmorhnivochas. 78 0
perhocus 347 0
potlt /hpes 5.567 2 Ngari 1:2,783
quinqunfkzsciltuji 73 0
thalasitus 1.097 0
tritaemorhenchus 20,08 1 2 Ngari 1:10,040
I Babanki 1:20,081
otntittaLtio group 5.565 2 Babanki 1:2,782
1 Bagaia 1:5,565
spp. 3,568 0
.1linswuo'a tgnid, rml.s 381 0
If, mit -',tsap p. I 0
*r anotaentias pp. 34 0
Total 62.055 20
All 'rust i-lalions were made from po s 0olu nfed females
NIM RR minimum field infection rate (n, ou %irus Tsolaies no of mosquitoes tested)
b%P RNT in Vero cells using NIH arbovirus ref- 15 isolates that reacted with BUN group refer-
erence grouping sera and type-specific imnt:une ence serum and showed similr patterns ofgrowth
mouse sera. Three isolates reacted poqitively with in Vero cell culture and suckling mice were placed
group A reference serum and with arti-Sindbis in group 2. The remaining two viral strains (16-
(SIN) mouse ascitic fluid. 15 isolates were mark- 17 and 20-100) that showed no reactivity in
edly inhibited by the Bunyamwera (BUN) se- PRNTs. but had similar growth characteristics.
rogroup reference serum, and two viral strains were placed in group 3.
(16-17 and 20-100) showed no reactivity with When assayed by the CF test. isolates in group
any of the immune sera used. Control viruses I showed antigenic similarity to one another and
showed positive reactivity with the appropriate to SIN virus. In contrast. results obtained with
antisera. other alphavirus antigens and immune sera (Chi-
Complement fixation test. Based on results ob- kungunya, Semliki Forest. Ndumu. and Mid-
tained from preliminary neutralization tests and delburg) showed virtually no reactivity when
characteristic growth patterns in cell culture and tested with group I viral strains. However. pre-
suckling mice. the viral isolates were categorized liminary results with neutralization tests of these
into different groups for screening by the CF test. viruses in mice showed close antigenic similarity
Group I consisted of three isolates (12-401, 20- to Babanki (BBK) virus.
130. and 22-17) that reacted with group A ref- All group 2 CF antigens reacted positively and
erence antiserum and with SIN ascitic fluid. The similarly when tested with immune serum pro-
746 GORDON AND OTHERS
TABLE 2 TABLE 3
Serohloc" identification(cid:127)a fisolate 20- l 00 hy the plaque- Serologic identil/cation o"i tolate 16- 17 h" viru~s neu-
rcdttction neutrali/ationt est tra.:atwon tesis in onue
Hypenmmune mouse ascitic fluid* Antigen*
Viral strain$ 20-100 Bagaza 16-17 iBangui
Antis(cid:127)era (6 It 1661t
20-100 >640 40
Bagaza >640 640 16-17 4.4f 3.3
Bangui 28 5.1
'Values are the reciprocal dilution inhibiting 80% of a plaque Jose ol
approsimatel, 50-10) plaque-forming units as assayed on Vero cell "Antigens were prepared from mouse bram.
monola-ers. t Values are the log, titer of antigen with normal mouse serum
t Virus was prepared from infe-ted Vero cell supernatants t Neutraliiation index (log., plaque-forming units of virus neutralized
with t(cid:127)pe-sp fcihacn tiserum).
duced against one of the isolates (14-144). All
isolates reacted positively with Ngari (NRI) type- in 1979 from male Ae. simpsoni mosquitoes
specific ascitic fluid. No group 2 antigen reacted reared from field-collected eggs.'" It has also been
with Germiston virus, but all antigens reacted previously isolated from .4n. gambiae s.l. in Bur-
with antibody to individual Ilesha. Shokwe. Bit- kina Faso and the Central African Republic. An.
ao. Mboke. and Bozo viruses when tested by the niascarensis in Madagascar, and Ae. argenteo-
CF test. punctatus. Ae. tittatus. and Ae. neoa/ricanus in
One group 3 antigen (20-100) reacted posi- Senegal."
ti-ely with Bagaza (BAG) virus immune serum. The numerous isolations in Fanaye Diern and
but did not react with other antisera to the Fla- the high minimum field infection rates in mos-
vivirus tested (Saboya. West Nile. yellow fever, quitoes in September 1988 suggest that NRI vi-
Zika. Spondweni. Uganda S. and Usutu). The rus was circulating at a high level. The August-
similaritv of 20-100 to BAG was confirmed by September 1988 rainfall was the highest in this
PRNT (Table 2). The other group 3 antigen (16- region since 1981. and Linthicum and others re-
17) did not react with any of the immune sera ported vegetation growth caused by rainfall in
tested, but did react strongly with Bangui (BGI) the Senegal River at this time to be almost as
Virus by the virus neutralization test (Table 3). extensive as in October 1987 when RVF virus
was found to be circulating at high levels.'
DISCUSSION The vertebrates involved in NRI virus am-
plification are unknown, although the virus has
Ngari virus was the most common isolate (I 5 been previously isolated from a sick sheep in
isolates), followed by BBK. (three isolates), and southern Mauritania."0 The numerous isolations
BAG and BGI viruses (one isolate each). Ngari of NRI virus from mosquito species that feed on
(Bulln'atvirus. Bunyaviridae) virus. registered with both humans and domestic ungulates (.-4n. gain-
the American Committee on Arthropod-borne liae. An. pharoensis. Cy. antennatus, Cv. poi-
Viruses in 1987, was isolated from six species: cillipes, and C~v. tritaeniorhtvnchus)" suggest that
in. pharoensis( seven). CX. antennatus( two). Cv.. human and domestic animal involvement in the
powillipcs (two). Cv. tritacniorhy-nchus( two).Ae. ecology of NRI virus should be investigated.
hirsuttus (one), and .-in. ganihiae s.I. (one). All Prevalence ofantibody to NRI in domestic sheep
isolates represent new mosquito-virus combi- in rural villages in southeastern Mauritania sug-
nations for Senegal. The majority ofisolates (II) gests that this virus was circulating in August
were collected in the village of Fanayc Diery. 1988.i' Serologic evidence from individuals liv-
while four were collected in Bode. Although both ing near Yonofere, Senegal indicate that humans
ofthese locations are in the vicinity ofareas where are infected with NRI virus.18
RVF activity was very high in the fall of 1987. Although NRI virus has been isolated in Ke-
we did not isolate RVF virus from mosquitoes.' dougou, Senegal, the isolations reported here are
Minimum field infection rates in Fanaye Diery the first in northern Senegal. Experimental stud-
wereas follows: .An. ganbiacs.l. (l:54)4,n. phar- ies are needed to evaluate the potential for .4-n.
nenltsl (1:89). CY. poicillipes (1:441). Cv. anten- pharoensis,w hich accounted for seven of 15 iso-
natult (1:1,062). and Cv. trtacniorht'nchus (1: lates. and other.4nopheless pp. to serve as vectors
1,976). Ngari virus was first isolated in Senegal of NRI virus. Investigations into the potential
ARBOVIRUS ISOLA(cid:127)TIONS FROM MOSQUITOES IN SENEGAL 747
for NRI virus to be transmitted transovarially Pasteur de Dakar for invaluable assistance in the field
are warranted based upon the initial isolation of' portion of this study. to R. E. Shope (Yale Arbovirus
Research Unit. New Haven. CT) for generous assis-
virus from males reared from field-collected eggs lance in virus identification, and to R. E. Harbach
and the isolation of the virus from adult female (Walter Reed Biosystematics Unit. Washington. DC)
Aedes spp., including the isolation reported here for identifying voucher specimens. We also thank J.
from Ae. hirsutus collected in Bode. 1' M. Dalrymple, J. E. Freier. K. Kenyon, G. W. Korch.
Babanki (Alphavirus, Togaviridae) virus, reg- T. P. Monath. and M. J. Turell for critically reviewing
the manuscript. This research was conducted in com-
istered with the American Committee on Ar- pliance with the Animal Welfare Act and other Federal
thropod-borne Viruses in 1987, was isolated at statutes and regulations relating to animals and exper-
three locations: Ndialene (in the delta region), iments involving animals and adheres to principles
Diongui, and Matam (approximately 400 km up- stated in the Guide fbr the Care and Use of*Laboratory
river). The virus was first isolated in 1969 from Animals. NIH publication 86-23, 1985 edition.
.1Iansoniaa fricanai n Cameroon and subsequent Disclaimer: The views of the authors do not purport
isolations have been made in Anopheles. Aedes. to reflect the positions of the Department of the Army
('i/ex. Eretmapodites. Coquillettidia.a nd 1atan- or the Department of Defense.
sonia species throughout much of sub-Saharan .Authors' addresses: Scott W. Gordon, Department of
Africa and Madagascar.`"' This is the first re- Microbiology. Colorado State University. Fort Collins,
ported isolation of BBK virus from Cv. tritae- CO 80523. Ralph F. Tammariello and David J. Dohm.
ntorhyrnchus and C.v. univittatus group mosqui- Department of Arboviral Entomology. Virolog\ Di-
toes. Babanki virus has been isolated from vision. U. S. Army Medical Research Institute of In-
fectious Diseases, Fort Detrick. Frederick. MD 21702-
humans: howcver, clinical disease was not de- 5011. Kenneth J. Linthicum, USAMC, AFRIMS,
scribed in association with these infections. Cal- Bangkok. Thailand APO AP 96546. J. P. Digoutte and
isher and others have reported that BBK virus M. A. Calvo-Wilson, Institut Pasteur de Dakar. PO
is closely related to SIN virus."' The BBK virus Box 220. Dakar. Senegal.
isolates used in this study were also found to be
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