Vol. 102, No. 1 Printed in U.S.A.

AMERICAN JOURNAL OF EPIDEMIOLOGY

Copyright © 1975 by The Johns Hopkins University

THE EPIDEMIOLOGY OF ST. LOUIS ENCEPHALITIS IN CORPUS CHRISTI, TEXAS, 1966 KENNETH H. WILLIAMS,1 F. BLAINE HOLLINGER,2 WILLIAM R. METZGER,3 CYRUS C. HOPKINS4 AND ROY W. CHAMBERLAIN5 Williams. K. H., F. B. Hollinger, W. R. Metzger. C. C. Hopkins and R. W. Chamberlain (Center for Disease Control. Atlanta, GA 30333). The epidemiology of St. Louis encephalitis in Corpus Christi, Texas, 1966. Am J Epidemiol 102:16-24. 1975.—In the summer of 1966. an epidemic of St. Louis encephalitis occurred in Corpus Christi, Texas, coincident with one occurring in Dallas about 563 km to the north. Among the 76 cases confirmed in Corpus Christi, there were two deaths; the attack rate was 41.0 per 100,000. In contrast with a concurrent outbreak in Dallas and the 1964 outbreak in Houston, attack rates were much higher in populations of the upper socioeconomic districts. This distribution may have resulted from the combined effects of an unusual concentration of vector mosquito breeding sites in storm sewers in the upper socioeconomic districts and a higher degree of residual immunity in the residents of the lower socioeconomic areas. arbovirus infections; encephalitis, St. Louis; mosquito control INTRODUCTION

An epidemic (SLE) occurred in the summer firmed cases of

of St. Louis encephalitis in Corpus Christi, Texas, of 1966. Seventy-six conSLE virus infection were

Received for publication November 7, 1974, and in final form March 3, 1975. Abbreviations: CF, complement fixation; CNS, central nervous system; HAI, hemagglutination inhibition; MVE, Murray Valley encephalitis; SLE, St. Louis encephalitis; ULV, ultra-low-volume; WEE, western equine encephalitis. 1 Viral Diseases Division, Bureau of Epidemiology, Center for Disease Control, Atlanta, GA. Present address: Departments of Psychiatry and Internal Medicine, University of Pittsburgh School of Medicine, Pittsburgh, PA 15261. 2 Virology Division, Bureau of Laboratories, Center for Disease Control. Present address: Department of Virology and Epidemiology, Baylor College of Medicine, Houston, TX 77025. 'Director of Public Health and Welfare, Corpus Christi-Nueces County Health Department, Corpus Christi, TX 78403. 4 Viral Diseases Division, Bureau of Epidemiology, Center for Disease Control. Present address: Department of Medicine, Massachusetts General Hospital, Boston, MA 02114. 5 To whom requests for reprints should be sent at: Virology Division, Bureau of Laboratories, Center for Disease Control, Atlanta, GA 30333. The authors wish to thank the many physicians, nurses, technicians and other persons in Corpus 16

identified; the attack rate was 41.0 per 100,000. This high rate was unexpected, since documented human infection with this agent had occurred in Corpus Christi residents in at least 7 of the preceding 11 years. Because of the relatively high attack rate in a city previously affected and because most cases occurred primarily among members of the upper and upper-middle socioeconomic classes, a pattern quite unlike that seen in a concurrent epidemic in Dallas (1), this epidemic was of unusual interest. This report summarizes the findings of epidemiologic investigations performed jointly during the outbreak by members of the Corpus Christi-Nueces County Health Department, the Texas State Department of Health, and a team from the Center for Disease Control (CDC). Christi, the Texas Department of Health, and the Center for Disease Control who contributed directly and indirectly to this investigation. They are particularly indebted to Dr. J. E. Peavy and the late Dr. J. V. Irons of the Texas Department of Health, Austin, Texas, for guidance, encouragement and support.

EPIDEMIOLOGY OF SLE IN CORPUS CHRISTI, 1966

17

cases were clinically and epidemiologically The city of Corpus Christi is located on evaluated by a member of the investigating the western coast of the Gulf of Mexico team, and appropriately timed serologic about 193 km north of the Rio Grande specimens were obtained for further testRiver, 290 km southwest of Houston and ing. Clinical classification. Clinical criteria 563 km south of Dallas. It has a semitropifor classifying the presenting illness were cal climate. based primarily on whether or not signs of Unlike the situation in Dallas, the spring meningeal irritation or central nervous sysof 1966 in Corpus Christi was neither tem (CNS) involvement predominated. On ecologically nor climatologically unusual; clinical grounds alone, every reported susheavy showers which inundated focal areas pect case was put into one of the following of northeast Texas in late April spared this four categories: encephalitis, aseptic menlow coastal region. ingitis, febrile headache, and "other" synThe city had been well aware of the dromes (including those cases in which undesirability of large mosquito populasymptoms were not compatible with CNS tions, partly because of emphasis on tourdisease). The definitions were the same as ism. Consequently, a mosquito control those used in evaluating the Dallas epiprogram, including draining and larvaciding of recognized pools of standing water, demic (1). Laboratory methods. The Texas State had been going on for several years. ObviDepartment of Health initially screened all ous breeding places such as open drainage sera by the hemagglutination-inhibition ditches at roadsides were treated regularly. (HAI) technique to determine activity Outbreaks of SLE in the Rio Grande against two arbovirus group B antigens, Valley had been previously described, and namely, SLE and Murray Valley encephathe general area was known to be favorable litis (MVE). MVE antigen is frequently for active virus transmission (2, 3). Docuused in group B arbovirus serology because mented cases of SLE had occurred in of its broad group reactivity which makes it Corpus Christi in 7 of the preceding 11 an excellent screening reagent. Later, in years, with small clusters of cases noted in retrospect in at least two of these years; the Texas State Department of Health however, no epidemiologic characteriza- laboratory and the Arbovirology Unit of tion of these outbreaks in the city was CDC, complement-fixation (CF) tests were conducted on these same sera. Serologic available. The 1966 epidemic was first recognized identification was confirmed by assaying in mid-August, when a physician saw three for neutralizing antibodies. The methods patients with recent onset of clinical en- used are described elsewhere (4). On the cephalitis and reported them to the Corpus basis of these laboratory determinations Christi-Nueces County Health Depart- and using the same criteria applied in ment. The Health Department subse- Dallas (1), cases were put in one of four quently initiated the epidemiologic stud- categories: confirmed, presumptive, inconies. In retrospect, July 8 was established as clusive, and negative, independent of prethe date of the first case of SLE in the area vious clinical evaluation. Population data. The population data and the beginning of the epidemic. used in the calculation of rates came from METHODS the 1960 US Census for the city of Corpus Suspect cases were tracked down and Christi and Nueces County. After the 1960 classified by a surveillance system similar census, Corpus Christi annexed three cento that used in the Dallas epidemic (1). All sus tracts in Nuece& County. The populaBACKGROUND

18

WILLIAMS E T AL.

tions of these three census tracts were added to the Corpus Christi figures to better estimate the population within the city's current geographic boundaries. The paucity of cases in the outlying rural areas of Nueces County and the marked ecologic differences between these areas and the city led to the arbitrary definition of the epidemic area as the city of Corpus Christi alone. The socioeconomic status of each census tract was calculated by the SerflingSherman technique (5). Prior SLE infections. Information on the city's past experience with SLE was obtained retrospectively by analysis of results in the files of the laboratory of the Texas State Department of Health in Austin. All cases for which sera were submitted for serologic study from 1956 to 1966 were reviewed, and the above-mentioned laboratory criteria (1) were applied to the results. When available, additional epidemiologically relevant data were obtained from these files, but no direct investigation of these patients was made. Investigation of mosquito vectors. Beginning on August 25 and continuing periodically until the latter part of October, mosquitoes in Corpus Christi were hand collected from daytime resting sites, just as they were in Dallas (1). As in Dallas, emphasis was placed on collecting the suspect SLE vector, Culex quinquefasciatus Say, and the method of collection and types of resting sites examined (chicken houses, sheds, porches, bridges, and culverts) biased the collections in favor of this species. It was apparent, however, that C. quinquefasciatus was the predominant mosquito breeding within the city area. Aedes taeniorhynchus (Weid.), a salt marsh breeder, is periodically a serious pest mosquito in the Corpus Christi area but was not abundant during the outbreak. Also, it is not known to be particularly susceptible to SLE virus or to serve as a vector. The collected mosquitoes were pooled

and tested for virus in the Arbovirology Unit of CDC by methods described elsewhere (6). RESULTS

In the course of the epidemic, which extended from July 8 to September 21, 258 patients with suspected CNS disease were reported to the Corpus Christi-Nueces County Health Department and were investigated as possibly having SLE. Of the 258 patients, 205 resided in the city of Corpus Christi and form the basis of this report. These 205 were classified as follows: 83, clinical encephalitis; 63, aseptic meningitis; 28, febrile headache; and 31, "other" syndromes (table 1). SLE was confirmed as the infection in 76 of the cases (37.1 per cent). Of the 76 confirmed cases, the clinical classification was as follows: 60, encephalitis; 14, aseptic meningitis; one, febrile headache; and one, "other" syndrome. The confirmed cases by week of onset are shown in figure 1. The peak occurred between August 13 and 20; thereafter a rapid decline was noted. Fifteen of the 205 suspect SLE cases were classified as presumptive. These cases were excluded from the present analysis because SLE infections in humans were known to have occurred in this area in previous years, and an inadequate number or spacing of specimens prevented specific TABLE 1

St. Louis encephalitis, Corpus Christi, Texas, clinical and laboratory classification of all reported cases July 10-September 24, 1966 Clinical category Encephalitis

Confirmed Presumptive Inconclusive Negative* Total

60 6 2 15 83

Aseptic

Febrile

gitis

ache

14 7 9 33 63

1 1 5 21 28

ither

1 1 3 26 31

T 76 15 19 95 205

* Including 11 cases with persistent titers in welltimed specimens.

19

EPIDEMIOLOGY OF SLE IN CORPUS CHRISTI, 1966 3O-i

TABLE 2

St. Louis encephalitis. Corpus Christi, 1966, age-specific attack rates, 76 confirmed cases

i— 20-

Cases (years)

Population

0-9

49,151 33,935 23,681 28,227 22,105 14,960 8,146 5,250 185,455

Male

Female Total

Attack rate per 100,000

10-

r

r-r-l

9

16 23 JULY

1—

30

~L_. 6

13 20 27 AUGUST

3

10 17 24 SEPTEMBER

WEEK OF ONSET

IGURE 1. St. Louis encephalitis, Corpus Christi, , 76 confirmed cases, bv week of onset.

10-19 20-29 30-39 40-49 50-59 60-69 70+

Total

interpretation of their positive SLE titers. In addition, 11 other patients had HAI or CF titers to SLE antigen, but showed no change in titer when appropriately spaced specimens were examined. These patients probably reflected SLE infection of a previous year and were classified as "negative." The 76 confirmed cases represent an overall attack rate of 41.0 per 100,000 for the Corpus Christi area (table 2). One unusual feature of this outbreak was the relatively high attack rates found among persons between 10 and 30 years of age (tables 2, 3). No reason was found to account for this age distribution. The incidence among females was higher than among males in the 20- to 40-year-old age groups, but the numbers were too small for statistical testing. Ethnic group and socioeconomic levels. The incidence of SLE in the white population with Spanish surnames (29.4 cases per 100,000) was significantly lower (p < 0.03) than in the rest of the white population (50.3 cases per 100,000) (table 4). The number of cases which occurred in the black population was too low to permit valid comparison. Attack rates were significantly higher in census tracts of upper and upper-middle socioeconomic classes than in the lower socioeconomic areas (table 5). It is not clear, however, that these effects were independent of geographic location.

4 9 4 1 3 5 5

3 5 9 8 7 4 3

7 14 13 9 10 9 8

14.2 41.3 54.9 31.9 45.2 60.2 98.3

2 33

4 43

6 76

114.3 41.0

TABLE 3

St. Louis encephalitis, Corpus Christi, 1966,* distribution of clinical syndromes by age Age group Encepr (years) alitis 0-9

10-19 20-29 30-39 40-49 50-59 60-69 70+

Total

6 9 8 7 9 9 6 6 60

gitis

Other

Total

0 0 0 1 0 0 0 0 1

7 14 13 9 10 9 8 6 76

ache

1 4 5 1

1 0 2 0 14

0 1 0 0 0 0 0 0 1

* 76 confirmed cases. TABLE 4

St. Louis encephalitis, Corpus Christi, 1966, incidence by ethnic group Attack Rate per 100,000 Ethnic group

White (non-Spanish surname) White (Spanish surname) Black Total

Population* Cases

Not

age-ad- Age-adjusted justedt

111,278

56

50.3

48.6

64,661

19

29.4

33.9

9,516 185,455

1 76

10.5 41.0

* Population data, US Census, 1960. t Age adjustments based on the age distributions shown in the 1960 census of Corpus Christi and associated census tracts affected by the epidemic.

20

WILLIAMS ET AL.

Geographic distribution. Figure 2 shows densely populated downtown areas, were the geographic distribution of the places of relatively spared. The residential southern residence of 74 of the 76 patients with half of the city, in census tracts of higher confirmed SLE. The north and northwest- socioeconomic area, had higher attack ern parts of the city, including the more rates, which suggests that in part the risk of acquiring SLE was a function of geoTABLE 5 graphic location. St. Louis encephalitis, Corpus Christi, 1966, attack Mortality. Only five deaths occurred rate by socioeconomic status of area of residence among all reported cases in Corpus Christi, and only 2 of the 76 patients with conAttack rate per 100,000 firmed SLE infection died. When only the Socioeconomic Population! Cases Not deaths in confirmed cases are considered, status* A the mortality rate for the city of Corpus justed justed Christi was 1.1 per 100,000; the case fatalUpper 46,313 24 51.8 51.3 ity ratio was 2.6 per cent. Both deaths Upper-Middle 44,502 28 62.9 64.6 occurred in patients in their 50's with Lower-Middle 48,631 19 38.4 39.1 clinical encephalitis. Lower 46,009 5 10.9 9.4 Total 185,455 76 41.0 Control measures. As in Dallas (1), aerial spraying by US Air Force C-123 Globemas* As determined by Serfling-Sherman technique ter aircraft with an ultra-low-volume (5). (ULV), high-concentration malathion mist t Population data, US Census, 1960.

Census Tracts, Socioeconomic Status ^

Upper 1

Upper-Middle

( 3 ) Lower-Middle ( ? ) Lower •

1966 Cases

® 1965 Cases FIGURE 2. St. Louis encephalitis, 1966, distribution of cases according to socioeconomic status of census tracts.

21

EPIDEMIOLOGY OF SLE IN CORPUS CHRISTI, 1966

was carried out at the rate of approxi- virus were made. Western equine encephamately 225 ml per hectare. In Corpus litis (WEE) virus was isolated twice, howChristi, however, it was apparently done ever, once from Culex tarsalis collected on too late in the epidemic (between August September 23 four weeks after spraying, 28 and September 1) for a depressing effect and once from C. quinquefasciatus colon the epidemic curve to be apparent or lected on October 7, six weeks after sprayevaluated. Also, the entomologic surveil- ing. No evidence of WEE infection in the lance was inadequate to assess fully the local human or equine population was effectiveness of the spraying in reducing apparent. the total vector population. The mosDISCUSSION quitoes were more difficult to find than in Dallas, probably due in part to the fact In the first reported urban epidemic of that easily accessible mosquito resting sites SLE in St. Louis, Missouri, in 1933, no (for the mosquito collector) were not as differences in attack rates in areas of differabundant, and prevailing winds made the ent socioeconomic status were observed, more open sites less favorable for mos- although attack rates were significantly quitoes. However, it was also apparent that higher in St. Louis County than in the city in the city as a whole the population of C. (7). Over the next 23 years several urban quinquefasciatus was lower than in Dallas. epidemics of SLE were recognized in sevNonetheless, from 604 C. quinquefasciatus eral areas (8-12). Although many of the mosquitoes collected 1 to 5 days before the epidemiologic patterns described in the aerial spraying, four isolations of SLE virus initial reports, such as the characteristic were obtained, yielding an infection rate of age distribution, were found to be repeated 1:151 (table 6). After the aerial spraying, in the subsequent epidemics, the socioecothe mosquito counts in many of the estab- nomic and geographic distribution of cases lished resting sites were reduced to 5-10 in each epidemic has varied, depending per cent of their previous levels for about largely on local circumstances. five days; and from the over 4600 C. Many of the epidemiologic features of quinquefasciatus collected over the next the earlier epidemics, such as the charactwo months no additional isolations of SLE teristic rise in attack rate in older age TABLE 6

St. Louis encephalitis, Corpus Christi, August 25-October 22, 1966, mosquitoes collected before and after aerial ULV spraying with malathion and tested for virus Species Aedes species* Anopheles speciest Culex quinquefasciatus tarsalis (Mel.) sp. Other speciesli Totals

1-5 days prespray 10 19

604*

ULV spray, Aug. 28-30

2

1

3

4

1 2

1

1 7

126

101

651

5 4 6

999

223H 124 757

1-9 weeks postspray

Grand totals

1 2

9 102

19 121

257 22 1 1 284

4628 1234

5232 1234

223 5

347 5

6201

6958

Weeks post-spray

4 133

41 143

36 695

34 1

1267

6

7

32

23

5

1030 688§ 586 333 589 55

190 12

2 24

85

17 1

1474 1327

5 1 670

g

9

1 208

* Species of Aedes and total numbers taken were aegypti, 1; taeniorhynchus, 10; thelcter, 8. t Species of Anopheles and total numbers taken were crucians, 16; quadrimaculatus, 75; pseudopunctipennis, 26; unknown, t Four isolations of SLE virus August 27, 28. § One isolation of WEE virus October 7. H One isolation of WEE virus September 23. U Other species of Culex taken were restuans, 4; salinarius, 1.

22

WILLIAMS ET AL.

groups, were again observed in Corpus Christi. The differences, however, deserve further comment. Some, such as the increased number of cases which occurred in persons between 10 and 30 years of age cannot be explained. The outbreak in Corpus Christi was in some ways similar to the one in Dallas, about 563 km farther north. Eoth epidemics began at about the same time and followed nearly identical temporal courses. However, the attack rate in Corpus Christi was more than twice that observed in Dallas (1), and in fact was much higher than in any other recently described outbreak of this disease (10-12). Although higher attack rates were reported from the first urban epidemics in St. Louis in 1933 and 1937, one should bear in mind that in those instances the diagnoses were made entirely on clinical grounds without laboratory confirmation (7, 8) and may have included many cases due to other causes. It has been suggested that the high attack rate in St. Louis in 1933 was the result of the introduction of a new viral agent into a totally susceptible population. The situation apparently was different in Corpus Christi, since at least isolated cases of SLE infection had occurred there over the previous 10 years. Evidence from two sources suggests that sporadic cases had previously occurred in Corpus Christi. Review of the files of the laboratories of the Texas State Health Department for the years 1955-1965 revealed at least one serologically confirmed case of SLE infection in each of 7 of the preceding 11 years (table 7). Small clusters of cases occurred in 1956 and 1965; these consisted of 5 and 10 confirmed cases, respectively. Furthermore, review of the discharge records of the two major hospitals serving the city disclosed that in 1956 and 1965 increased numbers of patients with a syndrome of "encephalitis" were admitted. Epidemiologic information was not available on most of these earlier cases;

TABLE 7

St. Louis encephalitis infections, Corpus Christi, 1955 to 1965 Year

Confirmed cases

Presumptive cases

1955 1956 1957 1958 1959 1960 1961 1962 1963 1964 1965

1 5 3 0 1 0 1 0 0 1 10

2 5 1 3 2 1 0 0 0 1 6

however, the geographic distribution of the residences of nine patients with confirmed SLE in 1965 are included in figure 2. Most of these cases occurred in the north and central lower socioeconomic portions of Corpus Christi and only a few in the southern upper socioeconomic sections of the city. Unfortunately, it was not possible to determine the locations of the residences of persons known to have had SLE before 1965. Because SLE infections had previously occurred in Corpus Christi, immunity acquired over the years may have served to protect inhabitants of the lower socieconomic areas during the 1966 outbreak. A subsequent serologic survey conducted by Hollinger in 1967 (13) showed a significantly higher proportion of persons in the lower socioeconomic areas to have antibodies to SLE than those in the upper socioeconomic areas of the city: 44 per cent (101/230) of people sampled (all age groups represented) in the lower socioeconomic zone had SLE antibody as compared with only 9.0 per cent (13/147) in the upper socioeconomic zone. The difference is highly significant (p =