<<

SrpreNrsrn, 1985 J. Au. Mosg. Corrrrnol Assoc. 305

THE IMPORTANCE OF AUTUMN RAINFALL AND SENTINEL FLOCK LOCATION TO UNDERSTANDING THE EPIDEMIOLOGY OF ST. LOUIS ENCEPHALITIS VIRUS IN INDIAN RIVER COUNTY, FLORIDA1

a JONATHAN F. DAY4 exo DOUGLAS B. CARLSON3

ABSTRACT. Culex nigripalpu adults were collected from sentinel chickens at 4 sites in Indian River Co. (IRC), Florida. Chickens located in well drained, open habitats attracted fewer Cx. nigripalpu than did those located in a moist, forested area, but the number of mosquitoes collected in the open habitats increased significantly with heavy autumn rainfall. All St. Louis encephalitis virus (SLE) seroconversions ( I l/674) during a7- period were from chickens located in open, well drained habitats. A comparison of monthly rainfall during of known SLE activity in IRC with the 22-year average showed that virus activity was significantly associated with years in which rainfall was unusually low in either or . Sentinal chickens in areas with large vector populations not be the most reliable indicators of local SLE activity and autumn rainfall in September and October may influence yearly SLE patterns in southern Florida.

INTRODUCTION virus (SLE) and eastern equine encephalitis virus (EEE) are enzootic and considered poten- Domestic and wild sentinel vertebrates are tial human pathogens. The bird-to-human often used to monitor specific areas for en- vector of SLE is Culex nigripalpzs Theobald cephalitis virus (Nichols et al. 1975, Dickerman (Chamberlain et al. 1964). The identity of the and Scherer 1983, Mclean et al. 1983). Adult bird-to-horse or -human Vector of EEE in chickens are the most commonly used sentinel Florida is still uncertain but Cx. nigripalpus may animals (LaMotte et al. 1967). Generally, from 2 be involved (Downs et al. 1959). to 24 birds are placed into secluded, all- Thirty Florida counties currently maintain , outdoor cages in areas where virus sentinel chickens to monitor areas for SLE and activity is suspected or known. These cages EEE. Some counties maintain sentinel birds in allow accessto field mosquitoes which, presum- the field all year. In Indian River County (IRC) ably, feed freely and, if infected, transmit virus 4 separate sites, each with 2 caged chickens, to one or more of the sentinel birds. Once a were maintained from through week one or more of the sentinels is bled on a July 1983. One bird from each pair was bled weekly rotating schedule, and the blood is checked in on a rotating schedule (King 1983) to minimize the laboratory for hemagglutination-inhibition the time lapse between bleeding and the final (HI) antibody to specific arboviruses. An HI report from the Florida Department of Health positive test (e.g., a rise in HI antibody titer and Rehabilitative Services Laboratory in from less than l:10 to greater than or equal to Tampa where blood samples were analyzed. l:40 on a single serum sample) indicates that Several factors determine the placement of the bird has been bitten by an infected mosquito sentinel flocks. They are placed: l) in areas and that virus is present in the area. In Florida where Culex spp. are known to occur com- all positive samples must be confirmed by a monly, 2) where they are easily accessible to second bleeding taken as soon as possible after mosquito control personnel for maintenance the positive results of the first bleeding are and weekly bleeding, and 3) where they are known. A severe shortcoming of this technique secluded to reduce the chance of vandalism- is that confirmation of a positive HI test may The day-to-day status of vector mosquito come many weeks after the infective bite, thus populations is not often considered when flock indicating past history in terms of virus activity sites are selected. In fact. little is known about in the area of the sentinel animals. mosquito presence and behavior at and around In southern Florida St. Louis encephalitis sentinel animals other than the indirect evi- dence of blood feeding or probing in the form positive I of virus seroconversions. Our purpose University of Florida, Institute of Food and Ag- in the present study was to use weekly aspirator ricultural SciencesJournal Series No. 6134. 2 collections to monitor resting adult Cx. nigripal- Department of Entomology, Fernald Hall, Uni- y'us at sentinel cages in 4 IRC locations. We were versity of Massachusetts, Amherst, MA 01003. 3 able to compare weekly mosquito Indian River Mosquito Control District, P. O. Box catches at 670, Vero Beach, FL 32960. each flock with the local rainfall at all 4 sites. We a Present Address: Florida Medical Entomology were also able to compare SLE virus activity Laboratorv. 200 9th Street S.E.. Vero Beach. FL during the 1978- 1984 seasonsat each site with 32962. the number of mosquitoes caught in 1983. 306 J. Ar"r. Mosg. Cournol Assoc. Vor-.I, No.3

MATERIALS AND METHODS ratory in Tampa where each was analyzed by HI test for SLE antibody. According to HRS SeNrrNnr- FLocKs. Indian River County is on policy any chicken which showed a four-fold the east coast of peninsular Florida with its increase in SLE antibody titer was bled again as center at 27'45'N, 80"35'W. In August- soon as possible for confirmation of SLE infec- November 1983, pairs of sentinel chickens were tion. maintained at 4 study sites in the county. The IRMCD sentinel chicken program began Site I was 6.4 km SW of Vero Beach in the in 1978, giving us 7 years of seroconversion center of a subtropical cabbage palm (Sabel data for each site (Table l). With these data we palmetto) lliv e oak Quercus virginiana) hammock were able to use a 2 x 2 test of independence surrounded by citrus groves. The ground and (using the G-statistic) to test for the association tree trunks in the hammock were covered with of habitat type and SLE seroconversions in In- Nephthrtisliberica of the aroid family. Site II,9.6 dian River County. km WNW of Vero Beach in a residential area, was in an open backyard. The only nearby for- ested area was 50 m to the east and was domi- Table l. Seven-yearrecord of SLE seroconversions nated by slash pine (Pinus elliottii). Daily rainfall in chickens at 4 sentinel flocks in Indian River data for sites I and II were collected bv the County, Florida. Florida Division of Forestry ar a station g.S km IRMCD sentinel flock number NW of site I and 6.4 km SE of site II. Site III was 14.4 km NNW of Vero Beach in a Year I] III IV Total % Positive live oak wood on an elevated sand ridge. Daily 1978 0124 0t24 0t24 0t23 0/95 0 rainfall data for this site were collected by per- 1979 0t22 v22 0t22 v2r 2t87 2.3 sonnel at MAAG Agrochemical Inc. 3.1 km SW 1980 0/33 2/33 0t33 3133 5n32 3.8 of the sentinel birds. l98l ot22 0t2t 0t2r 0t2r 0/85 0 Site IV was22.4 km NNW of Vero Beach in a 1982 0t20 0t20 0120 0n9 0t79 0 dense dwarf live oak (Quercus minima)lsaw- 1983 0t2r otzr 0t2r u2r U84 t.2 palmetto (Sermoa repens) habitat which was dry 1984 0/28 2t28 0t28 U28 3trr2 2.7 and open. Daily rainfall data for this area were Total 0/1705/169 0/169 61166 111674 1.6 collected nearby at the Florida Division of For- estry Roseland fire tower. The number of Cx. nigripalpru mosquitoes in 22-Yun. RATNFALLREcoRD. Daily rainfall data each weekly collection for each site was com- are collected by the National Oceanic and At- pared to the rainfall recorded for each site 48 mospheric Administration (NOAA) in Indian hr prior to the collection period using Kendall's River County at Vero Beach Laboratories (27o coefficient of rank correlation. 38'N, 80'27'W). Rainfall data from the Vero. Mosqurro coLLEcrIoNS. Resting mosquitoes Beach site, (as well as from other sites through- in and around each sentinel cage were collected out Florida) are published monthly in by power aspirator for 5 min per site once a Clirnatological Data. A 22-year (1963-84) week during the study period, usually on Friday monthly average of August-December rainfall mornings. The flocks were visited in the same for the Vero Beach station was calculated from sequence each week. Mosquitoes resting inside Climatological Data (Table 2). We were then able and immediately around the sentinel cages to compare August-December rainfall for were collected with a hand-held aspirator 50.8 1978-84 at the Vero Beach station with the cm long, powered by a l2V battery. The as- 22-year average to determine whether it was pirator had a diameter of 17.8 cm with a 43 cm above or below normal. where rainfall long, removable net bag made to fit inside. A exceeded the 22-year monthly mean plus the "wet." l2V direct current motor from Dayton Mfg. Co. standard deviation were defined as ran a fan which drew air and mosquitoes Likewise, months where total rainfall was less through the aspirator into the bag. The live than the 22-year mean minus the standard de- "dry" mosquitoes were returned to the laboratory, viation were defined as (Table 2). A 2 x 2 chilled, and the number of female Cx. nigripal- test of independence was used to examine the fru in each collection counted and recorded. association of unusually wet and unusually dry SLE eNrtsooy rDENTrFrcATroN.Once a week, Septembers and Octobers with the number of 3.0 ml of blood were collected from the wing SLE seroconversions for 1978-84. vein of I caged chicken; thus, each chicken was bled twice a . Blood samples were re- RESULTS turned to the laboratory, centrifuged, and the serums mailed to the Florida Department of Mosqulro coLLEcrroNS AT sENTTNELFLocKs. Health and Rehabilitative Services (HRS) Labo- Mosquitoes were consistently more abundant in SnrrnN{srn.1985 J. An. Mosq. Conrnol Assoc. 307

Table 2. Eight-year record of lndian River County, Florida, rainfall for August-December compared with 22 year (1963-84) mean rainfall and sentinelchicken SLE seroconversions.

No. IRC Monthly rainfall (mm) Seroconversions Year Aug. Sept. Oct. Nov. (Site) 1977 148.8 20r.7 56.6 81.5 169.7* Not done (l human-case) 1978 178.0 83.0** 81.3 I19.9 I 32.l* 0 1979 138.2 442.5* 41.9** 99.6 37.3 2 (II and IV) 1980 31.0** t82.4 39.1** 89.4 57,9 5 (2-rr,3-IV) 198l 463.8* 197.1 78.0 78.5 20.3*,r, 0 1982 238.8 187.7 78.5 297.4* 66.0 0 1983 230.4 81.3** 395.7* 40.1 109.7* l (rv) 1984 180.1 321.8* 92.4 346.7* 47.0 3 (2-rr,l-rv)

22-year mean 164.2 t97.7 146.0 89.9 59.2 (*SD) (85.7) (e6.3) (e4.6) (81.0) (42.6) * Unusually wet months (> 22-year monthly mean + SD). ** Unusually dry months (< 22-year monthly mean - SD). weekly collections from site I than from any of ber followed by an unusually dry October were the other sites.The mean (t standarderror) of associated with late October and November Cx. nigripalpw taken in weekly collectionsat the SLE seroconversions at sites II and IV. In 1980 4 siteswere: I - 288+48; II - 85126; III - an unusually dry October was associated with 2 42-+10;and IV - 39a I l. late October seroconversions at Site II and 3 at The relationship between the number of Cx. site IV. In 1983 an unusually dry September nigripalfus taken at each site in weekly collec- followed by an unusually wet October were as- tions and the rainfall pattern 48 hr prior to the sociated with a late October seroconversion at collectionis shown in Fig. l. There was no cor- site IV. In 1984 an unusually wet September relation between numbers of mosquitoescol- followed by a normal October were associated lectedand rainfall at site I, which wasa heavily with a late September seroconversion (site IV) vegetated forested area. Likewise, there was no and 2 early October seroconversions (site II). In correlation at site III, which was also a forested l98l and 1982 September-October rainfall was area. Mosquito collections were correlated with normal and no seroconversions were reported. rainfall patternsat sitesII (P < 0.05) and IV (P There was a highly significant (P < 0.001) posi- < 0.001) which were both well drained and tive association between September and Octo- open. ber rainfall patterns and observed seroconver- SLE ecrrvrrv AT IRc SENTINTI-rlocrs. 1978- sion patterns. Years where rainfall patterns 84. Sentinel chicken seroconversionsfor SLE during these months deviated from normal virus were recorded at 2 sites (II and IV) in were more likely to have virus activity. IRC since the surveillance program began in 1978(Table l). During this 7-yearperiod 5/169 DISCUSSION (3.|Vo\chickens seroconverted at site II, while 61166(3.6Vo) seroconverted at site IV. Both of The number of Cx. nigripa@ru mosquitoes these areas are open and well drained. There attracted to sentinel chicken flocks in southern were no seroconversionsat siteI (0/170)nor site Florida varied for the different habitats in III (0/169) which are both in woodland. Be- which the birds were located. The chickens tween 1978-84, 111674(l.6Vo) positive SLE penned in well drained, open areas attracted seroconversionswere recorded from sentinel fewer mosquitoes than those penned in moist, chickensin IRC. There wasa highly significant wooded areas. The proximity of flocks to the (P < 0.001)positive association between habitat larval habitat of Cx. nigripalpus is also an im- type and seroconversions during the 7-year portant consideration. Sites I, II, and III were study period with all of the seroconversionsoc- close to ditched citrus groves where Cx. nig- curring in the well drained, open habitats. riPaIPw commonly oviposited after heavy . INn-urNcr oF MONTHLy RAINFALLoN sLE Ac- Site IV was located several kilometers from Trvrry AT sENTTNELcHTCKENS rN rRc. Monthly suitable Cx. nigripalpu.r oviposition sites. rainfall patterns during September-November Even though fewer mosquitoes were collected appear to be important to the epidemiology of at sites II and IV than at site I, all of the SLE virus at sentinel chicken flocks in IRC 1978-84 SLE virus activity in IRC was recorded (Table 2). In 1979 an unusually rainy Septem- in these 2 open, well drained habitats. Fur- 308 J. Ar'r. Mosg. Coxrnol Assoc. Vol. l, No. 3

o SITE I srTEil l! 1. O.?7 'r=o.32 F f.= 1.7(ns) tr= 1.97(P

\ (J 200 a o z ta ' o a ir: 50 too t50 o 50 loo r50 RAINFALL (mm)

Fig. l. Plots showing the relationship between the number of mosquitoes captured and rainfall 48 hours prior to collection for IRC sites l-IV. Significance was tested using Kendall's coefficient of rank correlation. The t. values and level of significance are shown for each site (ns = not significant).

thermore, a significant association between the Martin County Department of Environmental number of mosquitoes collected at sites II and Services). There are several possible explana- IV and recent rainfall at those sites indicates tions for these observations: l) older mos- that mosquitoes depend on the presence of quitoes may be found in disproportionate and the resulting ground moisture to reach numbers in these open habitats. 2) After a rain- birds located in these open areas. Edman (1974) fall, gravid mosquitoes may fly into open areas suggested that autumn rain may be one cause of in search of an oviposition site or, after the observed feeding shift of Cx. nigripalpus ovipositing, may venture far to look for a host. from birds to mammals (Edman and Tavlor 3) These well drained, open sites may have an 1968). These autumn rains may allow the mos- associated SLE focus. quitoes to penetrate previously inhospitable, The reasons for sporadic SLE activity in dry habitats. We suggest that heavy autumn Florida are not clear. There are years like 1977 rainfalls enable mosquitoes to reach penned during which a widespread outbreak occurred hosts located in habitats which remain inacces- in central Florida. Associated with this outbreak sible to host-seeking vectors during dry periods were ll0 confirmed and presumptive human of the year. casesand 8 deaths (Chamberlain 1980). In 1978 The significant association between open, there was no SLE activity in Florida. We found well drained habitat types, low mosquito popu- SLE activity at sentinel flocks in IRC to be sig- lations, and positive SLE virus activity is sur- nificantly (P < 0.001) associated with unusual prising but not unique to IRC. Similar observa- autumn rainfall patterns (Table 2). In general, tions have been made in Sarasota County (per- when September or October were significantly sonal communication, Ron Winner, Sarasota drier than normal, SLE activity was recorded. County Mosquito Control) and Martin County Provost (1969) suggested that gravid Cx, nig- (personal communication, Lynn Erickson, ripalpus females may hold their eggs during dry Seprrvsnn. 1985 J. Au. Mosq. CoN-rnolAssoc. 309 periods and thus increase the probability that, References Cited when infected, the extrinsic incubation period Bond, O., D. T. Witte and H. C. Oard. blood meal J. Quick, J. J. would be completed before a second 1965. The 1962 epidemic of St. Louis encephalitis was taken. Our observations support this hy- in Florida. I. Epidemiologic observations. Am. J. pothesis. In IRC, years where September or Epidemiol. 8 I :392-404. October were unusually dry were more likely to Chamberlain, R. W. 1980. History of St. Louis En- be years with virus activity. During these dry cephalitis, pp. 3-61. In: T. P. Monath (ed.). St. periods (which lasted as long as 25 days) gravid Louis Encephalitis. Am. Publ. Health Assoc. Cx. nigripalpus may rest and wait for suitable Washington, D.C. H. Coleman and flying conditions (Dow and Gerrish 1970, Chamberlain. R. W., W. D. Sudia, P. L. D. Beadle. 1964. Vector studies in the St' Louis Provost 1974) or may simply not be able to find encephalitis epidemic, Tampa Bay area, Florida, suitable oviposition sites. If infected with virus 1962. Am. J. Trop. Med. Hyg. l3:456-461. by a recent blood meal, these mosquitoes caught Dickerman, R. W. and W. F. Scherer. 1983. Equine by unfavorable weather conditions would have herds as sentinels for Venezuelan equine en- plenty of time for the extrinsic incubation of the cephalitis virus activity, Nicaragua 1977. Bull. Pan. virus. Once rains create suitable oviposition Am. Health Org. l7:l't--18. sites, the mosquitoes would lay their eggs and Dow, R. P. and G. M. Gerrish. 1970. Day-to-day then host-seek as infective individuals. change in relative humidity and the activity of Culex Entomol. Soc. Culex nigripal4r,r is both an enzootic and an nigripalpus (Diptera: Culicidae). Ann. Am. 63:995-999. epidemic vector of SLE in Florida (Chamber- Downs, W. G., T. H. G. Aitken and L. Spence' 1959. lain et al. 1964, Bond et al, 1965). Virus activity Eastern equine encephalitis virus isolated from in sentinel flocks is observed most commonly Culex nigripalpzs in Trinidad. Science 130:1471. during September-November (Yeller 1978, Edman, J. D. 1974. Host-feeding patterns of Florida Nelson et al. 1983). Human SLE cases in mosquitoes. lll. Culex (Culex) and Culex (Neoculex). Florida usually occur in October or November. J. Med. Entomol. ll:9S-104. We found that in IRC SLE activity is signifi- Edman,J. D. and D.J. Taylor. 196S.Culexnigripalpus: cantly greater in sentinel chickens located in seasonalshift in the bird-mammal feeding ratio in a vector of human encephalitis. Science well drained, open habitats where mosquito mosquito l6 1:67-68. presence apparently depends upon autumn King, W. M. 1983. The use of sentinel birds for early rainfall patterns. We also show that SLE activity warning of mosquito-borne encephalitis in Dela- is significantly associated with years where ware l98l and 1982. Proc. 70th Annu. Meet. NJ. either September or October is unusually dry. Mosq. Control Assoc., pp. 137-141. Dry periods during these months may serve to LaMotte, L. C., G. T. Crane, R. B. Shriner and L. J. concentrate gravid vector mosquitoes which, Kirk. 1967. Use of adult chickens as sentinels. I. after suitable rainfall, ovipost and again host- Viremia and persistence of antibody in exper- seek. Likewise. after heavy rains parous mos- imentally inoculated adult chickens. Am. J. Trop. quitoes may be stimulated to long flights into Med. Hyg. 16:348-356. Mclean, R. G., Mullenix, Kerschner and J. drier areas seeking hosts. J. J. Hamm. 1983. The house sparrow (Passerdomesticus\ as a sentinel for St. Louis encephalitis virus. Am. J. Trop. Med. Hyg. 32:l 120-1129. ACKNOWLEDGMENTS Nelson, D. B., K. D. Kalpus, H. T. Janowski, E. Buff, F. M. Wellings and N. J. Schneider. 1983. St. Louis The Florida Medical Entomology Laboratory encephalitis-Florida 1977. Patterns of a wide- and Indian River Mosquito Control District spread outbreak. Am. J. Trop. Med' Hyg supplied space and equipment for this study. 32:412-416. We thank Charles W. Hansen for his technical Nichols, J. B., W.J. Bigler, E. B. Lassing and G. L. military dogs as assistance. We also thank Joe Spataro of the Hoff. 1975. An evaluation of sentry Florida Division of Forestry and Tom Bridges a sentinel system to Everglades virus (VEE FE 3-7C Mil. Med. 140:710-712. at MAAG Agrochemical Research Laboratory strain). Provost, M. W. 1969. The natural history of Culex for supplying us with daily rainfall data. nigripalpus. Fla. State Board Health Monogr. This research was supported in part by 12:46-62. Training Grant T32 AI-07109 from the Na- Provost, M. W. 1974. Mosquito flight and night rela- tional Institutes of Allergy and Infectious Dis- tive humidity in Florida. Fla. Sci. 36:217-225. eases,U.S.P.H.S. and by NIH Grant No. AI- Yeller, M. W. 1978. St. Louis encephalitis. J. Fla. Med. 1398l. Assoc. 65:577-579.