Plague in American Indians, 1956-1987
Allan M. Barnes, Ph.D. Thomas J. Quan, Ph.D. Mala L. Beard Gary O. Maupin Plague Branch Division of Vector-Borne Viral Diseases Center for Infectious Diseases
Bubonic plague (Yersinia pestis infection) is enzootic among native wild rodents and their fleas in much of the western United States from the Pacific coast eastward to about the 97th meridian (1). The disease in animals is characterized by sporadic or periodic epizootics among susceptible rodent populations, particularly members of the squirrel family (Sciuridae). Human cases acquired from wild rodents and their fleas result from chance encounters with plague-infected fleas or animals during epizootics, and cases typically occur as single, isolated events or in small clusters. In the past decade, approximately 19 cases per year have been reported. An apparently disproportionate number of these cases have occurred among American Indians (2,3). This report 1) presents information on the distribution of plague cases by racial/ethnic group and 2) discusses some of the factors believed to be responsible for the disparity. METHODS
All human plague cases reported in the United States are confirmed at CDC and reported to the World Health Organization (4). Records of case investigations since 1956 are on file at CDC and include information on race and other pertinent epidemiologic data. In addition to human plague, animal plague has been monitored with some consistency since 1970 in collaboration with various state and federal agencies that report animal epizootics and submit animal specimens as a plague surveillance activity (1). Surveillance activities include serosurveys for antibodies to Y. pestis among wild carnivorous animals and, particularly on Indian reservations, among domestic dogs. Such surveys reflect plague infection among rodent populations and provide information on the distribution and abundance of plague and its geographic and temporal ebb and flow. These epidemiologic and surveillance files were reviewed in this study of plague and its frequency among American Indians. RESULTS
Until 1965, when an outbreak of seven cases was reported from the Navajo Reservation in McKinley County, New Mexico, plague cases averaged one or two per year in the United States, and most of them occurred in the Pacific States (5). With the outbreak on the Navajo Reservation, plague cases began an increase that was centered in the southwestern states and that reached an average of 19 cases per year, with peaks of 40 cases in 1983 and 31 in 1984 (Figure 1).
Although plague in rodent populations is widely distributed and is reported frequently from 14 western states (Figure 2), most human cases are concentrated in the Southwest in an area that includes northern New Mexico, northeastern Arizona, and southern Colorado (Figure 2, Table 1). A similar concentration of cases is seen in California, southern Oregon, and western Nevada. In other areas, cases are infrequent or have never been reported. The center of distribution of human cases in the Southwest also is a center of distribution for American Indians and includes the 26,000-square-mile Navajo Reservation located in northwestern New Mexico, northeastern Arizona, and southernmost Utah.
In the period 1956-1987, 299 human plague cases were reported in the western United States. Most cases occurred in New Mexico (173 cases, 57.9%), followed by Arizona (43 cases, 14.4%), California (30 cases, 10.0%), Colorado (24 cases, 8.0%), and Oregon (10 cases, 3.3%). Scattered cases occurred in seven other western states, including Montana, which had its first case in 1987 (Table 1). The geographic distribution of cases from 1970 through 1986 and the distribution of animal plague detected by surveillance activities for the same period are shown in Figure 2.
Of the 299 persons who had plague in the study period, 91 (30.4%) were American Indians; 60 (20.0%) were Caucasian-Hispanics, mostly from north-central New Mexico; 146 (48.8%) were Caucasians from other states and New Mexico; one was Japanese; and one was Iranian. Of the 91 American Indians, 74 (81.3%) were Navajos and 12 (13.2%) were residents of various pueblos in north-central and western New Mexico. Cases also occurred on the Hopi, Mescalero Apache (New Mexico), Southern Ute (Colorado), and Warm Springs (eastern Oregon) reservations (Table 2). The attack rate among Navajos in 1983 was particularly high at 12.1/100,000 (2), when 19 cases were reported. During the same year, however, seven cases were reported from a predominantly Caucasian and Caucasian-Hispanic population in Santa Fe County in north-central New Mexico, for an attack rate of 9.3 (based on 1980 census figures for the entire county). Similarly, attack rates were 12.0 in Sandoval County in 1981 and 10.3 in Rio Arriba County, both in 1975 and in 1976. If the population data for Santa Fe were adjusted to eliminate the urban population from the calculation, the attack rate obviously would be higher. The data show that the risk of plague infection among the racially mixed, largely Caucasian and Caucasian-Hispanic population in north- central New Mexico is at least as great as that among Navajos (Figure 1).
The distribution of Indian patients by age group and sex (Table 3) and case-fatality rates closely paralleled those for U.S. plague cases in toto (Table 1). Fifteen of the 91 Indian patients died, resulting in a case-fatality rate of 16.5%. In comparison, 53 (17.7%) of the total 299 patients in the United States died. Most Indian patients were young: 31 (34.1%) were under 9 years of age, 20 (21.2%) were ages 10-19 years, and 12 (13.2%) were ages 20-29. The case-fatality rate, however, was remarkably lower (9.6%) in the less than or equal to9-year group than in older children and adults (20.0%). Distribution by sex was virtually even, with 47 male and 43 female patients. These figures closely parallel those for all U.S. plague cases, regardless of race; there is no evidence that American Indians are more susceptible than other races to infection, morbidity, or mortality from plague. In the instances in which the source of infection could be determined by epidemiologic investigation, no discernible difference was shown between cases among Indians and cases among other racial groups: available records for the period 1977-1986 showed that of the 62 cases among Indians, 41 (66%) were acquired via the bites of infective fleas, 14 (22%) resulted from direct contact with infected animals (rodents, rabbits, wild carnivores, or domestic cats), and 7 (11%) were of equivocal or unknown origin.
The number of plague cases in Navajo Indian populations each year appears to be proportionate to the scope and intensity of plague in animal populations. Plague surveillance on the Navajo Reservation includes annual spring surveys for plague antibodies among domestic dogs (1), an indirect measure of plague in rodents based on the fact that dogs become mildly infected, survive, and produce antibodies from ingesting infective rodent tissue. Data based on 680-1,400+ dog serum samples tested each year from 1983 through 1986 show that in 1983 (19 Navajo plague cases), 27.2% of all dogs on the Navajo Reservation that were tested had antibody titers of greater than or equal to32, and the geometric mean of positive titers (GMPT) was 247. In 1984 (four cases), 12.2% of dogs were seropositive, with a GMPT of 84; in 1985 (two cases), 4.2% were seropositive, with a GMPT of 58; and in 1986 (one case), 8.6% were seropositive, with a GMPT of 61. Although not directly comparable, surveillance data indicate that the data on dogs from the Navajo Reservation show a pattern of activity similar to that of human plague in the southwestern United States. The data indicate far greater plague activity in this region than similar serosurveys of dogs and wild carnivores have shown in other regions of the United States where plague is known to exist. DISCUSSION
American Indians, principally Navajos, have a disproportionate share of the plague cases reported in the United States (Figure 2). For example, in 1981, 1982, and 1983, 46.2%, 47.4%, and 52.5%, respectively, of U.S. plague cases occurred among Indians (5). Similar attack rates, however, have occurred among Caucasian-Hispanics and Caucasians in adjoining north-central New Mexico, thus indicating that the high incidence of plague is a regional problem rather than a racial one. A more accurate statement might be that plague is more likely to occur among persons who live in rural and semirural locations in the plague-focus area of the Southwest than among persons in other parts of the country.
One explanation for the concentration of cases in the region is that plague in animals and vector fleas is more abundant and occurs more frequently in the plague-focus area of the Southwest than elsewhere, as suggested by data from serosurveys of persons with plague and of dogs living on American Indian Reservations. Unfortunately, the denominator data needed for testing the hypothesis are lacking; no comparable data are available on serosurveys from other regions.
A second explanation has to do with the presence, often in large numbers, of plague-susceptible rodents and vector fleas. Among these are rock squirrels (Spermophilus variegatus) and their fleas, Diamanus montanus. Squirrels have a predilection for habitats created by human activity and often live peridomestically. Diamanus fleas bite humans readily and transmit plague effectively. Together, they are directly responsible for at least 41% of human plague cases in the United States (1). Prairie dogs (Cynomys gunnisoni) and their fleas, Opisocrostis hirsutus, also are widespread and abundant. Because of their abundance and susceptibility to plague, prairie dogs are a major amplifying host throughout the Southwest, including the Navajo Reservation. Prairie dog fleas are not inclined to bite humans, and most of the few cases acquired from prairie dogs follow the handling of a plague-infected animal, e.g., after preparing it as food. Human plague cases also have been acquired from various other hosts, including the antelope ground squirrel (Ammospermophilus leucurus) and its flea, Thrassis bacchi, resident in much of the Southwest. PREVENTION AND CONTROL
Efforts to maintain surveillance and to conduct prevention and control programs in the plague-focus area of the Southwest, particularly on the Navajo Reservation, are made difficult by the immensity of the region and the dispersal of its people. Health education on how to recognize and avoid plague is a principal program element of the Indian Health Service (IHS) and Tribal authorities. The message is carried by IHS and Tribal Community Health Representatives by word of mouth, by the Navajo Times, and by Navajo-language radio and television programs. Insecticidal control of vector fleas is carried out by the IHS in response to human cases or the finding of plague in animal populations where there is potential for human exposure. Each spring on the Navajo Reservation, a systematic serosurvey for antibodies to Y. pestis in dog populations provides surveillance data and a degree of prediction concerning the course of plague activity during the summer transmission season.
In north-central New Mexico, where human populations are more concentrated, plague remains a problem in Indian pueblos and other semiurban areas. In such areas, new stategies for preventing human exposure are expected to be effective. These include the preemptive application of insecticides and rodenticides to control flea vectors and rodent reservoirs where risk of human exposure is known to be high. Field trials of permethrin, an insecticide, and cholecalciferol (Vitamin D3), a rodenticide, have shown that these materials are safe and effective when used against rock squirrels and their fleas in New Mexico residential areas and pueblos (6). Applications have been made to register both materials with the Environmental Protection Agency and appropriate state regulatory agencies. Permethrin is expected to be equally effective against other species of flea vectors and in other situations; however, on the immense and thinly populated Navajo Reservation, the use of rodenticides and preemptive control measures is not indicated. Using control measures for vector fleas in response to human cases and maintaining surveillance to detect plague in animal populations will continue to be the primary strategy.
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