Great Basin Naturalist

Volume 39 Number 2 Article 1

6-30-1979

Review of in and the Great Basin

Harold E. Stark Environmental and Ecology Branch, U.S. Army , Dugway, Utah

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Recommended Citation Stark, Harold E. (1979) "Review of tularemia in Utah and the Great Basin," Great Basin Naturalist: Vol. 39 : No. 2 , Article 1. Available at: https://scholarsarchive.byu.edu/gbn/vol39/iss2/1

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ISSN 0017-3614

Volume 39 June 30, 1979 No. 2

REVIEW OF TULAREMIA IN UTAH AND THE GREAT BASIN

Harold E. Stark'

Abstract.— This is a compilation of tularemia research conducted in Utah, particularly at U.S. Army Dugway Proving Ground (DPG), Utah, and an evaluation of this information in relation to the current status of tularemia studies. A brief history of tularemia in Utah and a review of field and laboratory studies are included. Human cases of tularemia occur throughout Utah during all seasons of the year. An analysis of recent human disease reveals a concentration of cases in rural areas, with a greater seasonal occurrence in late summer and early

fall.

Research on tularemia as a zoonotic in- tularemia in recent years; Jellison and Parker fection in and around the U.S. Army Dugway (1945), Bell (1965), Olsuf'yev and Rodnev Proving Ground (DPG), Utah, has established (I960), Hopla (1974), and Olsen (1975) are the existence of natural foci of infection, cy- examples. In addition, several bibliographies cles of activity, and probable reservoir hosts have been compiled, e.g.: the U.S. Army and vectors. In addition, studies have been (1958), Hoogstraal et al. directed toward determination of survival (1970-1972), and Pollitzer (1967). Cox (1964), times of the organism as aerosols and as con- at Brigham Young University, prepared a taminants on surfaces in the laboratory and in "Bibliography of Tularemia" with references nature under varying field conditions. Field arranged by subject matter, similar to the one and laboratory work also have been con- published by the U.S. Army Chemical Corps. ducted at Brigham Young University and the Jellison was author (1950) and coauthor ; several species of deer fly (1945, 1951, 1956), of specific and general ar- (Chrysops spp.) were found infected in na- ticles on tularemia (many of them on tula- ture. remia in Utah), and he prepared a current re- view and bibliography on tularemia (1974). Human tularemia is commonly a rural dis- Much of the information given here is a re- ease, probably with an eight-year cyclic ten- view of large quantities of data from DPG re- dency in Utah. It is transmissible to man ports and records not ordinarily available to through direct contact with the host, con- the scientific community. Since the data are tamination of water and food, vectors, in- voluminous, not all can be analyzed; many halation of dust as from tick feces while DPG reports and articles are referenced for shearing sheep, and, uniquely in the Great further analysis (if desired) by the reader. Basin, by the bite of deer flies. Other portions of this work constitute a liter- There have been several review articles on ature survey.

'Environmental and Ecology Branch, U.S. Army Dugway Proving Ground, Dugway, Utah !

103 104 Great Basin Naturalist Vol. 39, No. 2

History ance and display varying pathogenesis. Bio- chemical reactions (glycerine fermentation The etiologic agent of tularemia, Franci- and the presence or absence of citruUine sella tularensis, was not identified until this ureidase) have been related to virulence century (McCoy 1911, McCoy and Chapin (Marchette and Nicholes 1961). Some strains have ap- 1912). However, tularemia may resist streptomycin. Eigelsbach, Braun, and in rural Utah. pared earlier among humans Herring (1951), Skrodsky (1966), and Domin- physician, Pearse (1911), a Brigham City owska (1967) observed a correlation between studied six human cases of an imknown dis- the colonial morphology and the pathogeni- ease which occurred in August 1908 in the city and immunogenic properties of a given area. It is believed Brigham City-Tremonton isolate. to be the first clinical description of tula- Based on virulence, chemical reactions, remia in the English language. Pearse left the morphology, geographic origin, epizootiol- disease unnamed. Later medical accounts re- ogy, epidemiology, vectors, reservoirs, associ- viewing epidemiologic and clinical aspects of ation of different habitats, and modes of the disease assumed deer fly bites were asso- transmission, two basic subspecies of tula- ciated with it, although no infected insects remia have gained recognition. These are were captured or identified. commonly referred to as types A and B (Bell Francis, another physician, first isolated F. 1965). Subspecific designations also have tularensis from wild mammals and their ecto- been made referring to types A and B. The parasites in detailed 1919 and conducted less virulent of the two is palaearctica (Type studies near Holden in the Delta area of Mil- B) and is more frequently associated with ag- lard County (Francis 1921, 1927). Before ricultural areas and lotic waters, and may be ' referred the disease as "Pahvant 1920 he to maintained by chronic tularemia nephritis in Valley plague" and "deer fly fever." Later muskrats, beavers, and voles. Voles may be established the tula- (1921) he and used name the primary reservoir in some areas in west- remia for the disease. Simpson (1929) wrote a ern North America. Chronically infected ver- textbook on medical aspects of the disease, tebrates urinate onto watersheds, sometimes assembling knowledge to that time. He asso- causing widespread and protracted human the cases in largely with deer fly ciated Utah epidemics (Bell and Stewart 1975). bites. Human infection with palaearctica has oc- curred during threshing operations in the Etiologic Agent USSR. Possible similar occurrence of human tularemia in the Great Basin is discussed later

Francisella is distinctive and only distantly imder tularemia in soils. Another proposed related to other bacterial organisms. Buchan- name, holarctica, for Type B, implies that an and Gibbons (1974) gave no hierarchical this type occurrs throughout all land masses arrangement for it. The genus is placed with of the Northern Hemisphere. Though holarc-

Brucella, to which it is not closely related," in tica is less restrictive in concept, palaearctica a group of genera of uncertain affiliation en- has taxonomic priority. Francisella t. tula- titled "Gram-negative aerobic rods and coc- rensis (Type A, also designated F. t. nearc- ci." There has been no general compilation tica) is more virulent and is frequently associ- of strains published to date, although there ated with infection in lagomorphs (hares and are significant differences in levels of viru- rabbits) and nonaquatic (xeric or mesic) ro- lence among strains of F. tularensis. Yet viru- dents, more frequently involves human cases lence alone does not provide a basis for clas- contracted during hunting, and is often asso- sification, because under laboratory culture ciated with vectorborne transmission than is and storage it can change. Different labora- palaearctica (Bell 1965). tory hosts express different levels of resist- Besides the currently recognized sub-

'There is some serologic cross reaction between F. tularensis and Brucella (Hopla 1974, Quan 1978). June 1979 Stark: Review of Utah Tularemia 105 species, two additional nomenclatural desig- Hamilton, Montana, preserves numerous nations have been proposed, }aponica (Ro- strains by lyophylization, but effort is not de- dianova 1967) (for Japanese isolates) and voted to identification and cataloging; it is mediasiatica (Aikimbaev 1966) (for a central more convenient to obtain fresh material Asian strain). Aikimbaev (1966) and Olsul'yev from nature for ongoing research. (1970) regard the latter as primitive. Aikim- Storage and preservation or cultivation (es- baev proposed subspecific status for media- pecially in egg yolk) in the laboratory reduc- siatica. Taxonomic status has not been eval- es virulence of the organism (Owen 1970). uated for either of these two names. Green (1943) increased virulence of unnamed The tularemia organism in nature is ubiq- strains of F. tularensis by passage through uitous, but simultaneously demonstrates cottontail rabbits and hares. On the other ubiety with regard to strain differentiation. hand, he contended that passage through Numerous strains have been recognized. grouse reduced virulence. Owen et al. (1961) These often have been designated with num- failed to enhance the virulence of F. tula- bers or initials. At DPG, nine strains are rensis by experimentally passing strains maintained and studied: Jap 4, Ohara, Live through hosts or ectoparasites. Some strains Vaccine, S. C, Russ, Max, 38, 38A, and Schu have considerable vitality for sustaining their 5. Similar groups have been kept at several characteristics. There are great variations of educational institutions, the U.S. Public virulence in strains isolated in nature. Older Health Service, Rocky Mountain Laboratory literature on virulence refers to resistance, at Hamilton, Montana; Centers for Disease susceptibility, and mortality in human in- Control at Fort Collins, Colorado, and At- fections. No assignment of strains, even as far lanta, Georgia; and at several state health de- as types A or B, is possible for these old isola- partments. Several strains may occur in one tions. No classification or cataloging of F. locality (e.g.. Prince George County, Vir- tularensis strains appears possible at the pres- ginia, where several strains came from a ent time. Buchanan and Gibbons (1974) sug- single species of tick—Haemaphysails lepo- gested a nomenclature that has had partial rispalustris). Karlsson et al. (1970) and Karls- acceptance at best. Thus, resolving the status son and Soderlind (1973) obtained 50 strains of the number and identity of the strains of F. from a limited area in Sweden; most of these tularensis (other than the two principal came from a single species of tick. Many types) remains an unresolved problem. publications list strains collected locally from laboratory. In nature or developed in the Research on Tularemia in Utah Stoenner et al. (1959) and Marchette and AND THE Great Basin, 1945-1975 Nicholes (1961), the strains DPG-1,2,3,4,5,6, SKV- 1,2,3, and 9-K-161 are reported as iso- Table 1 summarizes research on tularemia lates from ticks {Dermacentor parumpertus, in nature in the Great Basin. These in- Hemaphysalis leporispalustris, and others), vestigations are discussed in the following cottontails {Sylvilagus audobonii), and jack- section. Krinsky (1976) devoted about half of rabbits (Lepus californicus) around DPG. his review of tularemia in tabanid flies (Chry- Marchette et al. (1961) listed 18 cultures kept sops spp.) to the historical occurrence of tula- at DPG and at the University of Utah, Salt remia in nature in Utah and to research pub- Lake City. A staff report on tularemia at lished by Utah-based authors. Krinsky's high DPG (No. 88U; USA-DPG 1962b) listed 26 regard for studies of tularemia in Utah strains (18 from DPG) used in susceptibility prompted an expanded review. and vector studies of transmission. There is Distribution, reservoirs, and cycles in no record of preservation of these isolates. nature.— The occurrence of tularemia in Some strains are preserved in adjacent states. Utah differs from that in other parts of the Dr. of the Plague Branch of et al. believed F. Thomas J. Quan world. Rodenwaldt (1952) the Communicable Disease Center, Fort Col- tularensis to be ubiquitous in the Holarctic lins, Colorado, has strains SKV-2 and DPG-1 Realm and to occur in permanent and well- as part of his F. tularensis collection. Mr. defined epicenters where it is maintained, Scott Stewart, Rocky Mountain Laboratory, and from which it may spread. The area from 106 Great Basin Naturalist Vol. 39, No. 2

Table 1. Summary of basic research on tularemia in the Great Basin, 1945 to 1975.

Principal Investigators' Date Institution^ Subject of research

Jellison, 1945 RML Parker

Jellison 1950 RML

Jellison, Kohls, 1951 RML Philip

Jellison, Kohls 1956 RML

Rodenwaldt 1952 U.S. Navy

Woodbury, 1953 Parker

Woodbury

U of U staff

Philip, Bell, Larsen

Allred, Stagg, Lavender

Stagg, Tanner, Lavender

Parker, Johnson

Vest, Marchette

Stoenner, Holdenried

U of U staff

Parker, Olsen, Dolana

E&E staff

Lundgren, Marchette, Nicholes

ditto

Gebhart, Thorpe June 1979 Stark: Review of Utah Tulahemia 107

Arkansas to southern Illinois constitutes one Several species of deer fly are the principal major epicenter in North America. Another vectors to man from zoonotic sources (possi- well-defined epicenter exists in the western bly infected hares) in Utah. Throughout the part of the continent, of which Utah (espe- remainder of the world, ticks and sometimes cially the Delta area) is a part. Later pub- mosquitoes (Rodenwaldt et al. 1952) are the lications attach no particular significance to principal vectors to man. Other sources of these epicenters of tularemia as defined by human tularemia infection include contact Rodenwaldt et al. Maximov (1960), however, with the infected hosts, contaminated water, regarded tularemia as an important natural or aerosols. regulator of rodent hosts and reported that it Tularemia appears to occur widely in a va- occurs in favorable foci in the USSR as re- riety of environments and hosts. Few areas lated by the concept of "landscape epide- are as ecologically diversified as Utah. Tula- miology." remia is widespread from the Great Salt Lake Jellison and Parker (1945) proposed that Desert to the Uinta Mountains. It has trans- cottontails (Sylvilagus spp.) are basic reser- mission cycles involving waterborne tula- voir hosts responsible for 90 percent of hu- remia, as with muskrat trappers around Utah man tularemia in North America. Lake (Jellison, Kohls, and Philip 1951); air-

Thorpe, Marcus, Sidwell 108 Great Basin Naturalist Vol. 39, No. 2 borne tick feces as with sheep shearers (Jelli- the specimens. In contrast, high rates were son and Kohls 1956); direct contact, as with found for carnivores and livestock, usually rabbit hunters; and deer fly bites as with 26 greater than 11 percent, while moderate of 170 laborers at Locomotive Springs, Utah rates were recorded for deer and wild horses. (Burnette 1936, Hillman and Morgan 1937). Greater risk of exposure, longer lives, innate These latter authors reported that laborers resistance, and persistence of antibodies may removed their shirts while working, that sick account for higher occurrence in these mam- jackrabbits were seen in the area, and 13 men mals as opposed to rodents. The incidence of were known to have killed jackrabbits or antibodies was usually similar in widely dif- handled dead ones. The locations of initial ul- ferent groups of hosts in the same year. For cers of the shoulders and backs of the work- example, in 1965 22 percent of 651 cattle men suggested, however, that jackrabbits samples were positive, 42 percent of 1,579 were not directly involved as a source of hu- sheep samples were positive, and 25 percent man tularemia. of 31 carnivore samples were positive. In Francisella novicida was isolated and de- 1968 the proportions of samples with anti- scribed from Ogden Bay, on the eastern side bodies to F. tularensis were small: 0.03 per- of the Great Salt Lake (Owen 1974), and has cent for rodents, 2 percent for livestock, and never been reported elsewhere. Thus Utah 3 percent for carnivores. In other years carni- differs from all other areas of the world by vores persisted with high rates, and rates in harboring all three recognized taxa of Franci- other animals were low. For example, in sella. 1970 antibody rates were 4 percent in sheep, Epizootiology of tularemia at DPG.— 0.4 percent in cattle, percent for rodents, In 1951 a program was begun to study and and 17 percent for carnivores. Antibody re- analyze plants and animals at DPG and adja- coveries from rodents and jackrabbits re- cent areas (Woodbury 1956, 1964). Emphases mained consistently small however, sugges- were placed on enumerating enzootic path- ting that rodents play a minor role in ogens as well as potential introduction of oth- maintenance. Also of little significance to the er pathogens to determine possible vectors maintenance of F. tularensis in nature is the and routes of natural dissemination. Most re- jackrabbit, which is very susceptible and suc- search on tularemia at DPG was conducted cumbs promptly. This observation may ex- under contract. Reports entitled "A Study of plain why few jackrabbits in nature possess the Ecology and Epizoology of the Native antibodies to tularemia. Fauna of the Great Salt Lake Desert" (An- A special summary report prepared by the nual Summaries 1951-1969) were published Ecology and Epizoology research staff, Uni- by the University of Utah (USA-DPG versity of Utah, summarized DPG studies on 1951-1969). "Ecology Studies of Western host relationships for ticks, lice, and fleas Utah" 1971-1973 were prepared by EcoDy- (USA-DPG 1962b). The report discussed ex- namics Incorporated (Desert Test Center perimental vector transmission studies that USA-DTC 1971-1973). From 1969 through included immunization and susceptibility ex- 1964, special summary reports on tularemia periments using several strains of F. tula- were published as DPG in-house reports. rensis on laboratory mice, rabbits, guinea These voluminous reports contain much raw pigs, and deer mice. Isolations from wild data in tables and graphs. Additional tabula- mammals, birds, and livestock were tabu- tion, study, and synthesis of data are not lated. Ecological observations on biotic com- within the scope of this review. The follow- munities and population dynamics, particu- ing provides a cursory summary of some re- larly for the jackrabbit, were summarized. sults. Serologic methods for detecting antibody ac- From 1951 through 1979 evidence of tula- tivity, especially agglutinating, complement- remia existed in virtually all 46 areas of Utah fixing tests, and cutaneous responses were re- in which specimens were collected and from viewed. Some of the information in this re- 35 areas sampled routinely. Serologic evi- port has not appeared in published literature. dence of the organism was found infrequently Stagg, Tanner, and Lavender (1956) pro- from rodents, usually in less than 1 percent of duced experimental infection of F. tularensis June 1979 Stark: Review of Utah Tularemia 109

in jackrabbits, seven species of rodents, and maximum virulence. One viable organism coyotes (Canis latrans). They found that coy- sufficed for a lethal dose in laboratory rab- ote pups were less susceptible to tularemia bits, mice, hamsters, and guinea pigs. Olsen than rodents. Infection of rodents via con- and Dolana ([EcoDynamics, Inc.] USA-DTC taminated food was difficult. When infection 1971-1973) provided additional support to of rodents and jackrabbits was successful (as Stagg, Tanner, and Lavender (1956), March- from aerosols), the disease usually progressed ette et al. (1961), and Thorpe et al. (1965).

rapidly to death (3-5 days). Olsen and Dolana found that (1) F. tula- Gebhardt and Thorpe (1962) presented a rensis isolated from most hosts near DPG tabular review of worldwide vectors and usually had maximal virulence, but occasion- hosts. The pathogen, vectors, hosts, epide- al isolations had little virulence; (2) carni- miology, epizootiology, and control were giv- vores were readily infected but recovered en a generalized interpretation. Thorpe et al. and did not demonstrate a carrier state; (3) (1965) reported on tularemia studies from cottontails were su.sceptible to infection; and

their inception at DPG (1951 through 1964). (4) jackrabbits were more susceptible than Areas of study included the Bonneville Basin cottontails. Klock, Olsen, and Fukushima of western Utah and adjacent portions of Ne- (1972) obtained eight isolations of F. tula- vada, where 35 areas were sampled semi- rensis from Chrysops discalis, Dermacentor annually or quarterly. During the 13-year pe- panimapertus, H. leporispalustris, and jack- riod 52 isolations of F. tularensis were made, rabbits from four areas near DPG (Delta,^ approximately half from wild mammal tissues losepa, Callao, and Gold Hill). Tests of viru- and half from ectoparasites. The authors also lence showed all eight to be typical Type A

tabulated information on human tularemia (nearctica), which is virulent for laboratory from 1941 through 1964. This information, mice and rabbits. EcoDynamics personnel updated with data from the Utah State Divi- ([Olsen and Dolana] Desert Test Center 1971 sion of Health, is presented in this article as Annual Report [USA-DTC 1972]) were mys-

Figure 1 and is discussed later in the section: tified by the large numbers of seropositive

"Distribution of Recent Cases of Tularemia cottontails near Delta because tularemia is in Utah." Isolation data with respect to live- imiformly fatal to cottontails. They hypoth-

stock, wild mammals, birds, and their ecto- esized that (1) Delta cottontails were some- parasites and collections of positive sera were what resistant to F tularensis as a result of

also tabulated. Six local epizootics were ob- selection pressure, or (2) the detection of the served during the 13-year period. Tissue iso- antibody was a nonspecific reaction, or (3) an lates were made from jackrabbits, which aviRilent strain of F. tularensis (present in were collected in great abundance, one cot- the area) was responsible for the antibody ti- tontail, and four rodents. Serum agglutinins ters. They found support evidence that there were found in birds, wild mammals (includ- probably were specific and protective anti- ing deer), and livestock (roughly 25 to 30 bodies for cottontail rabbits in the Delta percent of the serum samples tested). Most area. Selected details of these supportive data isolates possessed maximal virulence; how- are given later imder "Hosts." On the basis of ever, two isolates from the cottontail and a their findings, the EcoDynamics staff (1972) Great Basin pocket mouse (Perognathus par- questioned the validity of the generally ac- vus) were of low virulence. Thorpe et al. in- cepted concept (based primarily on viru- dicated that strains from North American lence) of types A and B for F. tularensis. Ol- nonaquatic hosts and ectoparasites are some- sen and Dolana conjectured further that times of lower virulence. neither type is limited to specific habitat Vest et al. (1965), in a five-year study of types nor to specific animal groups. They enzootic diseases in Utah, reported that 10 stated that types A and B allow synthesizing strains of F. tularensis were isolated from la- the bewildering array of strains into an gomorphs and rodents. All strains were of epizootiological pattern. No alternative

barriers between the two areas. 'Delta, 97 air km (60 air miles) from Dugway, is not physically near, but is environmentally similar with few 110 Great Basin Naturalist Vol. 39, No. 2 method for organization or cataloging was Epidemiology group, suggested a potential offered. health hazard from Chnjsops spp. Krinsky Olsen (1975) reviewed some of the Great (1976) pointed out that isolations from deer Basin surveys by DPG abstracted in the pre- flies in Utah in 1965, 1968, and 1969 provid- ceding paragraphs. He noted that the major- ed evidence of the potential importance of ity of isolations of F. tuhrensis came from these tabanids in the dissemination of F. tula- jackrabbits and its primary tick parasite (D. rensis, even though they are regarded as parumapertus), but agglutinins were detected short-term mechanical vectors. After these in 22 percent of blood samples from cattle isolations, EcoDynamics researchers made and sheep. Of interest is the decline in rate of net collections of tabanids and later sugges- recovery of evidence of the tularemia organ- ted epidemiologic associations with human ism in nature from 1954 to 1970. The major- cases ( Annual Reports, ity of isolations were made earlier with com- USA-DTC 1971-1973). Klock, Olsen, and paratively little change in field collecting Fukushima (1973) suggested the same associ- effort. This suggests wide and long-term vari- ations (discussed later in this review). Philip ation in the amoimt of pathogen circulating (1968) found that another tabanid (Tabanus in native reservoir hosts and vectors of the punctifer, may have been associated with a area. human case reported near Battle Mountain, Epidemiology of tularemia around Nevada. DPG.- Klock, Olsen, and Fukushima (1973), Parker (1957) and Parker and Johnson who described an outbreak of tularemia in (1957) attempted the transmission of F. tula- 1971 near Delta and Grantsville, Utah, stud- rensis by fleas in the laboratory. In one at- ied the epidemiology of 39 human cases with tempt, three species of fleas were infected, investigations of vectors, hosts, and incidence but none of them transmitted F. tularensis to of isolations from specimens collected. Nine- a susceptible host. In another attempt, Or- teen of these human cases suffered deer fly chapeas leucopus transmitted F. tularensis to bites, and another nine reported insect bites a specimen of Peromijscus treui. Extensive by imknown species. The pathogen was iso- studies on transmission of tularemia by ticks, lated from hosts and vectors in both areas overwintering, and transovarial passage of and adjacent areas such as Skull Valley, Utah. the pathogen have been conducted at Rocky Also, there was an epizootic among la- Mountain Laboratory in Hamilton, Montana gomorphs. F. tularensis was isolated from tis- (Jellison 1974). Vector studies of tick trans- sue of jackrabbits and cottontails. Because of mission are reported in the University of unusually large numbers of midges (Leptoco- Utah Ecology and Epidemiology Annual Re- nops spp. and Culicoides spp.) observed in port (USA-DPG 1962b). Otohius lagophilus, 1971, the authors suggested that these might removed from a dead jackrabbit, transmitted have played a role in the human outbreak. F. tularensis to cottontails and to a domestic Vectors.— Cox (1965), in a study on F. white rabbit (Oryctolagus spp.), the first tularensis and deer flies in the environs of known transmission by this tick. Twenty-two Utah Lake, isolated the organism from Chry- species of ticks were recorded from DPG and sops spp. in nature for the first time. Experi- environs, of which five species (Dennacentor mental transmissions by C. discalis was dem- andersoni, D. parumpertus, Ixodes kingi, Hae- onstrated by Francis and Mayne (1921). Cox's maphijsalis leporispalustris, and Otohius lago- isolation of F. tularensis from C. fulvaster philus) were infected with F. tularensis and C. aestuans demonstrated that species (Johnson 1966, Thorpe et al. 1965, and An- other than C. discalis (this common species nual Reports USA-DPG 1962-1969). It is was only suspect before that time) are vec- conceivable that, in the Great Basin, the tick tors. Knudsen, Rees, knd Collett (1968) isolat- and jackrabbit (D. parumapertus and L. cali- ed F. tularensis from C. discalis, thus associ- fornicus, respectively) constitute a polyhostal ating the bite of C. discalis with a human reservoir (Hopla 1974:47). case. Other isolations of F. tularensis from deer flies from near the Great Salt Lake, Hosts.— Marchette et al. (1961) demon- made by the University of Utah Ecology and strated the susceptibility of locally captured June 1979 Stark: Review of Utah Tularemia 111

wild mammals to tularemia. Eleven species sponse of partially resistant hosts (such as lab- of wild rodents and cottontails were very sus- oratory rats and cottontails). ceptible. Some species of wild rodents {Ony- The EcoDynamics group (USA-DTC 1972) chomys leucogaster, Perornyscus maniciilatus, reported that 54 carnivores (41 percent) had and Neotoma sp.) were very susceptible to significant levels of hemagglutinins for F. virulent strains but were resistant to the tularensis. This group of carnivores included "38" avirulent strain. Carnivores {Taxidea 52 bobcats {Lynx rufus), 19 badgers {Taxidea taxiis, Vulpes macrotis, and Canis latrans) taxus), 8 skunks {Mephitis mephitis), 19 coy- were readily infected orally; the infection otes {Canis latrans), 30 kit foxes {Vulpes soon was no longer demonstrable, and the an- macrotis), and 2 domestic cats {Felis domes- imals did not become carriers. The authors ticus). The positive specimens came from the concluded that tularemia in the Bonneville 13 collecting areas around DPG. A more sen- Basin is a disease primarily of jackrabbits, sitive hemagglutination technique was devel- with the cycle in nature maintained by that oped in the early 1970s. Therefore, the high- host and the vector {Demiacentor paruma- er percentage of serum samples with pertus). The authors also concluded that agglutinins found from 1970 to 1972 (11 per- Lepus spp. were more susceptible than Syl- cent), may be expected to have higher vilagus or Oryctolagus. The published con- (though not significantly higher) values when clusions of these authors differ from the gen- compared to those calculated from tube ag- eral concept throughout the Annual Reports glutination testing from 1960 to 1969 (USA-DPG 1964-1969) that jackrabbits are (roughly 8 percent). The two tests (tube ag- so susceptible that they play a minor role in glutination, later replaced by micro- maintenance. The snowshoe hare (L. ameri- agglutination, and hemagglutination) are dis- caniis; European counterpart—L. timidus) is cussed later under "Methodology." less susceptible than jackrabbits or Minnesota The phenomenon of carnivorism among Sylvilagiis spp. to infection with F. tularensis rodents is well known in literature for both (Green 1943, Green, Larsen, and Bell 1939). dissemination and maintenance of plague and Marchette et al. (1961) noted that L. c. tularemia. Vest and Marchette (1958) fed car- deserticola was more susceptible than L. c. te- casses of 119 rodents {Perornyscus spp.) in- xianiis. fected with F. tularensis to 11 species of ro- About half of 19 cottontails (S. aiidobonii) dents (squirrels, heteromyids, and cricetids). captured near Delta showed no demonstrable In all cases, every rodent that ingested in- levels of antibody to F. tularensis (EcoDy- fective flesh contracted tularemia. Some spe- namics Inc. USA-DTC 1972). However, 9 cies (mostly heteromyids) were reluctant to survived the challenge inoculation of 83 cells feed on flesh, but did so when starved. The of F. tularensis; they had developed high lev- extent to which wild rodents supplement els of antibodies. Subsequently, an isolate their natural diet with flesh was not deter- from cottontails from Delta was tested on mined. other cottontails collected from Delta and Cabelli, Ferguson, and McElmury (1964) Gold Hill. All of the experimental hosts from and Cabelli et al. (1964) reported that the

Gold Hill died, suggesting that some of the mourning dove {Zenaidura macruora) is rela- Delta cottontails were naturally "immu- tively resistani- to F. tularensis, but the au- nized" with an avirulent strain of F. tula- thors speculated that fecal transmission could rensis. This natural avirulent strain may have be significant in dissemination of tularemia to been responsible for previously observed susceptible birds. It is of interest that, when a seropositive cottontails (31 percent of 62 Schu strain of F. tularensis was administered specimens) collected near Delta in 1972 to several species of oceanic birds by several (USA-DTC 1972). EcoDynamics concluded routes, few transmissions from infected to that Delta cottontails may possess some in- susceptible birds were observed. Francisella nate resistance to certain strains of F. tula- tularensis, however, was found in the bird ex- rensis. However, much more work needs to creta although no other evidence of disease be done to clarify the relation, if any, be- (bacteremia) was noted. The brown noddy tween lethality of various strains and the re- {Anous stolidus), whitecap noddy (A. min- 12 Great Basin Naturalist Vol. 39, No. 2 utus), white tern (Gygis alba), and sooty tern moisture in the soils at the time of in- (Sterna fuscata) were susceptible to infection. oculation was the single most important fac- Infection in these birds was achieved by res- tor for survival. Survival of the organism was piratory or cutaneous pathways, rarely by the better below the surface. Subsequent wetting oral route. increased survival. Exposure to sunlight was Host immune system.— Thorpe and Mar- deleterious. The maximum times after in- cus (1962, 1964a,b, 1965a,b,c, 1966, 1967) oculation that tularemia organisms could be and Thorpe, Sidwell, and Marcus (1964) re- recovered from the soil were 90 days in win- ported on the implication of phagocytosis in ter and 35 days in summer. When conditions F. tularensis infections. They determined that were adverse (as in summer heat), survival the phagocytic system of the immune mecha- was as short as a few hours. nism functions as importantly as the antibody An interesting problem has been reported system for resisting and overcoming in- from USSR by Olsuf'yev and Rodnev (1960). fections. Tularemia infection of humans is acquired by Studies of F. tularensis in soils and the pulmonary route while harvesting cereal ON fomites.— At DPG research and testing crops. Crops were apparently contaminated was conducted on F. tularensis to charac- by infected F. t. palearctica, and human in- terize its aerosol stability and persistence in fection resulted from inhalation of dust raised soils and on fomites. Many observations and into the air from contaminated straw and experiments were conducted by DPG Life grain. These conditions are reported to have Science Division that were apart from studies caused mass infections in people processing by contractor groups to DPG such as the the harvest (Spendlove 1974). Popek et al. University of Utah and EcoDynamics, Inc. (1969) reported that washing sugar beets con- and in-house field work by the Environmen- taminated by infected rodents in a sugar beet tal and Ecology Branch. Most specific studies works in South Moravia created aerosols that on F. tularensis were highly specialized and infected 237 people over four harvesting sea- printed as numbered reports (other than sons. To date, similar events have not taken USA-DPG 1951-1969, USA-DTC 1971-1973, place in the Great Basin. Waterborne tula- USA-DPG 1976, 1978, and University of remia did infect human beings in Oregon Utah contract reports). The primary purpose during a meadow mouse population explo- of field-related work (referenced above) was sion (Jellison, Bell, and Owen 1959). A poten- to study the nature and geographic distribu- tial for airborne infection of tularemia exists tion of tularemia occurring naturally in the throughout the Great Basin whenever thresh- DPG area. An additional purpose was to ing or harvesting operations occur. monitor the potential for intrusion or estab- lishment of tularemia relative to test activi- Methodology ties. Both laboratory and field studies of aero- sols were conducted from the early 1950s Serology.— With the basic technique of through the late 1960s. Many facts were re- Alexander, Wright, and Baldwin (1950), the ported concerning F. tularensis in nature. staff of EcoDynamics and their predecessors Unfortunately, this information read- was not developed a highly sensitive hemagglutina- ily available to the scientific community at tion (HA) test. Dr. Bruce Hudson at the Pub- large. Many of these documents are now lic Health Service, Center for Disease Con- available through interlibrary loan. trol, Fort Collins, Colorado, assisted in An experiment by Thome (1966) is per- preparing lipopolysaccharide extract of F. tinent to this presentation. pre- Three tularensis for sensitizing sheep cells. This dominant soils of the area (sand dune, DPG method is currently used at DPG. Tube ag- clay flat, and salt flat) were inoculated with glutination (TA) was replaced by micro- F. tularensis. The pH of the three soil types agglutination (MA) in 1977. Hemagglutina- varied but little (7.5-7.9). In general, sand tion (HA) was first tried by EcoDynamics in dunes were the least favorable for preserva- 1970, and this test replaced TA in 1972. tion of F. tularensis, this probably because Duplicate samples were tested in 1973 and soil dried out faster than the other two. High 1978. According to the 1973 Annual Report June 1979 Stark: Review of Utah Tularemia 113

(USA-DPG 1976:89-94 and Table 44), testing technique in identifying 54 strains, 4 from by untanned sensitized sheep erythrocytes man and 50 from natural hosts (mostly hares was more sensitive to the presence of anti- and ticks) in Sweden. They found that once bodies to F. tularensis than was testing by ag- techniques have been established in a given gkitination of a stained antigen (MA) by anti- laboratory, histopathologic examination was bodies in unknown samples. The simplified, and the hazard of laboratory- polysaccharide sensitized sheep cells are acquired infection was reduced. The IF more likely to yield false positive tests. method was successful for identifying tula- Today the more sensitive HA test is used as a remia in decomposed material. Cutaneous al- screen and second confirmation, and the less lergic reactions and IF techniques are two sensitive MA test is used as a final con- promising methods for identifying current firmatory test. In all replicates MA and TA tularemia activity in human and other mam- tests gave similar results and TA has been dis- mal populations around DPG. continued. A technique for sampling tabanids for Recovery of pathogen from infected F. tularensis.— Knudsen, Rees, and Collett ARTHROPODS.— Improvements in techniques (1968) described a trap designed to obtain are presented in the 1973 Annual Report large numbers of deer flies and other tabanids (USA-DPG 1976). Though the passive HA for surveys for the tularemia organism. The micro-test became firmly established, dis- trap is pyramidal, about 1 m high and 1 m cussions of other methods in earlier Annual across the base. About midway up the Reports (USA-DTC 1971-1973) merely al- triangle face on either side is a rectangular lude to more recently developed methods. flapped opening for flies to enter. Once in-

One of these is the hemolymph test (Burg- side, the flies can enter a funnel (20 cm diam- dorfer 1970), in which the distal end of a tick eter) against the tip of the pyramid. The top leg is cut and the hemolymph collected on a of the funnel is closed but has small openings slide, stained with immunofluorescent or oth- around the perimeter. Some of the flies inside er dye, and examined. This method was dis- the funnel may fall through the narrow end, cussed in some detail in the 1971 Annual Re- through a plastic tube into a styrofoam box port (Deseret Test Center USA-DTC 1972). beneath containing 4 to 8 kg of dry ice, However the test has not been used at DPG. which freezes the flies. The sublimation of Skin test for evidence of tularemia.— carbon dioxide also serves as an attractant Cutaneous allergic reactions have been de- and is the only bait used. During one season veloped for the diagnosis of tularemia in ro- (1968), Knudsen, Rees, and Collett trapped dents and rabbits (Lundgren, Marchette, and 1,248 deer flies (C. discalis) from marshes Nicholes 1961, 1962). Cutaneous sensitivity bordering the southeastern shore of the Great was elicited by inoculating as few as 10 F. Salt Lake. Isolates of F. tularensis were ob- tularensis cells; sensitivity was demonstrable tained from flies trapped in this manner. for 25 to 53 weeks, depending on species. This diagnostic test aids in establishing pre- Recent and Current Projects vious infection with tularemia for wildlife species. Buchanan, Brooks, and Brachman During 1974 and 1975 personnel at DPG (1971) reviewed the use of skin tests for hu- further improved the hemagglutination test, man clinical identification of tularemia and which had proved valuable for the staff of epidemiologic studies. Human reactors may EcoDynamics. Lipopolysaccharide antigen remain hypersensitive for as long as 40 years. was prepared for serologic examination of Antigen prepared for a human skin test (but wildlife and livestock serum specimens col- suitable for use on hosts such as jackrabbits) is lected around DPG. The macroagglutination available at the Center for Health and Envi- test has been replaced by a micro- ronmental Studies at Brigham Young Univer- agglutination test in accordance with Massey sity. and Mangiafico (1974). Owen (1974) de- Immunofluorescence.— Karlsson et al. scribed morphology and characteristics of F. (1970) and Karlsson and Soderlind (1973) re- tularensis and provided information useful in viewed the use of immunofluorescent (IF) growing and identifying isolates. 114 Great Basin Naturalist Vol. 39, No. 2

With these recently improved techniques Great Basin) by Lane and Emmons (1977). it has been reconfirmed that low levels of an- They concluded that human cases have grad- tibody occur in serum samples taken from ro- ually decreased since 1927, and they theorize dents and lagomorphs and a higher incidence that the cause was urbanization and selective occurs in serum samples from carnivores. As pressures that have resulted in a decreased presented in preceding annual reports (USA- virulence of organisms maintained by reser- DPG 1951-1969), sera from a few wild voir species. A gradual decrease is not evi- horses at DPG were nearly all positive, but dent from data on human tularemia collected generally antibody response in livestock var- from Utah, but urbanization correlates with a ied. A greater percentage of sheep seem to decrease of incidence of tularemia as in Cali- possess tularemia agglutinins after a stay on a fornia. There is a periodic resurgence in time distant summer range than sheep bled during that may be more marked in Utah than in the winter around DPG. Curiously, speci- California. mens of deer serum contributed by hunters in 1973 possessed no demonstrable antibody, DiSTRIRUTION OF ReCENT HuMAN CaSES though response in deer had been high during some previous years. The Communicable Disease Section of the Incidence of tularemia in wildlife around Utah State Division of Health has kept re- DPG will be reviewed in future publications. cords of reportable diseases, including tula- The first will deal with jackrabbit population remia, for many years. With their permission, changes and tularemia. There has long been recent records representing current condi- an assumption that population reduction of tions have been tabulated and are presented jackrabbits is somehow associated with out- as part of Figure 1. Thorpe et al. (1965) and breaks of tularemia in nature. During the last Jellison (1974) have assembled records of 13 years quantitative data have been collect- tularemia cases through 1964. Jellison's for- ed around DPG which support the general mat has been used here with additional de- observation that the jackrabbit is subject to tailed information included. large changes of a cyclic nature. While dying In Figure 1 the number in each county on jackrabbits infected with F. tularensis have the upper right is 1 percent of the human been found, the organism or the disease it population in 1977. The number on the up- produces has not been proved responsible for per left is the total cases of tularemia report- a widespread decline in jackrabbits. For ex- ed from 1941 through 1977 (37 years). The ample, Philip, Bell, and Larsen (1955) record- larger figure in the center of the county is ed infected Dermacentor parumapertiis from the number of tularemia cases per 100,000 infected jackrabbits during a peak in the pop- persons per annum, averaged for 37 years. ulation cycle of these lagomorphs in Nevada. The ratio between the total number of cases Firm evidence that tularemia was responsible in each county and the 1977 population of for eventual decline of the population was each county was analyzed with a posteriori not demonstrable. There appears to be simul- test by simultaneous testing of the homoge- taneous association of pathogen activity (e.g., neity of sets of replicates for goodness of fit evidence of antibodies) from cattle, sheep, (G-Statistic, Sokal and Rohlf 1969). Ten sets carnivores, cottontail rabbits, jackrabbits, and of samples (under "maximum nonsignificant rodents. There also seems to be an inverse ranges" in Table 1) were homogeneous; that correlation with jackrabbit density, particu- is, no ratio within each of these sets was sig- larly the marked decline of jackrabbits in the nificantly different at the 5 percent level of DPG area (definitely evident in 1973). At confidence. The counties which are indicated that time there was an apparent increase in as significantly higher under "exclusive tularemia activity. This event followed rather ranges of homogeneous ranges" overlap with closely the increase of activity of F. tula- no ratio included in the low group. Ratios in rensis in all indicator species during the early Table 2 are expressed as average cases per 1970s. 100,000 per annum on the map. Three mral Epizootiologic and epidemiologic studies counties, Daggett, Millard, and Rich, had val- were conducted in California (outside the ues above 15 per 100,000. Seven more rural of Utah Tularemia 115 June 1979 Stark: Review

county - Large number in center of incidence per 100,000 human "^ * " ,^°_^ population. left ot ;?.v.vA\v^v.':\V7Avrv:v7.v.' fiT' ;22 "aal^^j^ Small number in upper fc-82iS^ tularemia. county = no. cases human right of Small number in upper x luu. = human population r//.v/.v.v.\\v.v.\v.v.v.v.v.v.v.v.v.-.v.v.v.v.v. ^^^ county ' -' " ' <^S ITTAFI

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tularemia, 1941 through 1977. Fig. 1. Incidence of human 116 Great Basin Naturalist Vol. 39, No. 2

counties, Beaver, Carbon, Duchesne, Emery, Sanpete, Uintah, and Wasatch, had values above 7 per 100,000. Counties with the low- est values (less than one per 100,000), Davis, Weber, Morgan, and Salt Lake, are located along the Wasatch Front, which has dense human population (except for Morgan Coun- ty). Washington County also has a very low value. The average for the entire state of Utah (1941 to 1977) is 1.66 cases per 100,000 per annum. Figure 2 shows the actual number of known cases in Utah by year from 1960 through 1977. Two periods of increase above average occurred during the years 1961 through 1964 and 1969 through 1971. Values less than 10 were experienced from 1965 through 1968, and the high of 1971 was fol- lowed by a series of values which were low- est for the longest departure from the aver- age for 1972 through 1977. Distribution of cases by month for the 17

years preceding 1978 is shown in Figure 3. These cases represent date of report, not date of onset or contact with sources of infection. In most cases contact would occur about a month earlier, making the lowest three

Table 2. Homogeneity of sets of replicates tested for goodness of fit.

Ratio: Maximum Exclusive Ranges Cases Nonsignificant of Homogeneous Pop. Ranges Ratios

Daggett June 1979 Stark: Review of Utah Tularemia 117 jackrabbits in maintenance and transfer of mer Plague Laboratory in San Francisco and tularemia is poorly understood. Serum speci- at DPG indicate that fleas are probably not mens with high titers are most frequently vectors. found among carnivores, which apparently To improve our knowledge of epizootiol- do not develop overt symptoms but maintain ogy of the disease, one needs a clearer under- antibodies to F. tiilarensis for a long time, standing of the role of jackrabbits in trans- and livestock that are exposed to vectors. As mitting tularemia and whether tremendous with jackrabbits, the part that carnivores and fluctuations in population density affect fre- livestock have in epizootiology of tularemia quency of transmission. Also needed is a is unclear. Although some birds are suscep- knowledge of strain differences and whether tible, the pathogen passes from birds with viRilence changes in a given area over a peri- difficulty. They probably play no role in. od of time. Finally, a determination should epizootiology in the Great Basin. Levels of be made of the regression and subsequent oc- serum agglutinins among various species of currence of tularemia during apparent inter- mammals correspond well both geographi- epizootic times with regard to geographic cally and in time. As the antibody levels rise sites, ecologic niches, and primary hosts and slightly ix} rodents and lagomorphs, a con- vectors. Because of the variety of conditions comitant increase is found in serum samples under which the disease occurs, Utah appears of carnivores and livestock. Tests by the for- to be a prime area for study.

40

30

60 65 70 75 77 YEAR

Fig. 2. Annual occurrence of tularemia in humans in Utah, 1960-1977. 118 Great Basin Naturalist Vol. 39, No. 2

Acknowledgments References Cited

Appreciation is expressed to the following, AiKiMBAEV, M. A. 1966. Taxonomy of genus Francisella. who offered advice and consultation during Izv. Akad. Nauk Kazakh SSR, s. Biol. 5:42-44. Alexander, M. M., G. G. Wright, and A. C. Baldwin. the preparation of the manuscript: F. Bell, J. 1950. Hemagglutination using Franciselhi {Pas- Edwards, G. L. Choules, G. T. Crane, T. W. tularensis polysaccharide. Exptl. teurella) J. Med. T. Fukushima, A. T. Hereim, C. E. Hopla, 91:551-556. W. L. Jellison, W. L. Krinsky, P. S. Nicholes, Allred, D. M., D. E. Beck, and L. D. White. 1960. Ticks of the genus Ixodes in Utah. BYU Sci. Bull., Quan, H. B. Rees, C. F. A. Pinkham, T. J. Jr., Biol. Ser. 1(4): 1-42. M. A. Rothenberg, L. L. Salomon, J. C. Allred, D. M., G. N. Stagg, and J. F. Lavender. 1956. Tipton, and C. M. Wheeler. Spendlove, V. J. Tularemia. Experimental transmission of Pasteu- Dr. Pinkham suggested the study of human rella tularensis by the tick, Dennacentor parinna- ].lni.Dis.99:U3. tularemia by statistical analysis and used a pertus. American Public Health Association. 1964. Diagnos- program which he prepared. Initial stages of tic procedures for rickettsial diseases. APHA., this accoimt arose from a research grant pro- New York. Chp. 1, p. 54-55. Dr. Tipton. F. 1965. Ecology of tularemia in North Ameri- posal prepared by Bell, J. ca. Medicine 2:33-44. Research on which this report is based was J. Jinsen Bell, F., and S. Stewart. 1975. Chronic shedding supported by Department of Army Project J. J. tularemia nephritis in rodents: possible relation IT0061101A91A (In-House Laboratory Inde- to occurrence of Francisella tularensis in lotic pendent Research). Dis. 11:421-4,30. waters. J. Wildl.

J F M A M J J

Fig. 3. Monthly occurrence of tularemia in Utah, 1961-1977. June 1979 Stark: Review of Utah Tularemia 119

Buchanan, R. E., and N. E. Gibbons. 1974. Bergey's Jellison, W. L. 1950. Tularemia: Geographical distribu- Manual of Determinative Bacteriology. Williams tion of "deer fly fever" and the biting fly Chry- & Wilkins, Baltimore, Maryland. 1246p. sops discalis Williston. Pub. Hlth. Rpts. Buchanan, T. M., C. F. Brooks, and P. S. Brachman. 65:1321-1329. 1971. The tularemia skin test: 325 skin tests in 1974. Tularemia in North America. 276p. Univ. 210 persons: Serologic correlation and review of of Montana Foundation, Missoula, Montana, also, the literature. Ann. Int. Med. 74:336-343. U.S. Army Med. Rsch. & Dev. Com., Washing- Burgdorfer, W. 1970. Hemolymph test: A technique ton, D.C., Contract DADA-17-73-C-307D. L., F. R. 1959. for detection of rickettsiae in ticks. Jellison, W. J. Bell, and C. Owen. The Amer. J. Trop. Med. Hyg. 19:1010-1014. Oregon meadow mouse irniption of 1957-1958. Burnett, T. W. 1936. Tularemia in a Rocky Mountain Mou.se disease studies. Bull. Ore. State College, sector of the western front. Military Surgeon p. 71-80. 78:193. Jellison, W. L., and G. M. Kohls. 1956. Tularemia in V. E. sheep and in sheep industry workers in western Cabelli, J., W. Ferguson, and R. C. McElmury. 1964. Tularemia: Experimental infection in the United States. PHS. Publ. 421, Pub. Hlth. Mono. mourning dove. Zoon. Rsch. 3:93-98. 28; also Bull. Hyg. 31:517p. V. F. A. Jellison, W. L., G. M. Kohls, and C. B. Philip. 1951. Cabelli, J., Hodapp, E. W. Ferguson, and M. Peacock. 1964. Tularemia: Potential for trans- Tularemia: Muskrats as a source of human in- 48:594-597. mission by birds. Zoon. Rsch. 3:99-124. fection in Utah. Rocky Mtn. Med. J. Jellison, W. L., and R. R. Parker. 1945. Rodents, rab- Cox, K. B. 1964. Bibliography of tularemia (published bits and tularemia in North America; some zoo- by Cox, Provo, Utah). 83p. logical and epidemiological considerations. Am. 1965. Tularemia and deer flies in the environs of 25:349-362. J. Trop. Med. Utah Lake, Utah. Great Basin Nat. 25:13-29. Johnson, D. E. 1966. Ticks of Dugway Proving Ground Dominowska, C. 1967. Properties and typing of Franci- and vicinity and their host associations. Proc. sella tularensis colonies. Inst. Marine Medicine. Utah Acad. Sci., Arts, and Lett. 43:49-66. Gdansk 19:131-154. In press. Transmission of Pasteurella tularensis by EiGELSBACH, H. T., W. Braun, AND R. Herring. 1951. the argasid tick Otobius lagophilus. Studies the variation of Bacterium tularense. on J. Karlsson, K. a., S. Dahlstrand, E. Hanko, and O. Bact. 61:557-570. SoDERLiND. 1970. Demonstration of Francisella Francis, E. 1921. The occurrence of tularemia in nature tularensis (syn. Pasteurella tularensis) in sylvan as a disease of man. Pub. Hlth. Rpts. animals with the aid of fluorescent antibodies. 36:1731-1738. Acta. Path. Microbiol. Scand. Sekt. B, 1927. History of tularemia. DeLamar Lecture, 78:647-651. In: Studies on the immunofluores- School of Hyg. and Pub. Hlth., Johns Hopkins cent technique as a diagnostic tool in bacteriol- Univ., Baltimore, Maryland, p. 94-115. ogy. (Karlsson, ed., 1975). National Veterinary In- 1928. A summary of tularemia. Medicine. stitute, Stockholm. 7:411-432. Karlsson, K. A. and O. Soderlind. 1973. Studies of the 1937. Sources of infection and seasonal incidence diagnosis of tularemia. Contributions to micro- of tularemia in man. Pub. Hlth. Rpts. 52:103-113. biology and immunology. 2:224-230. In: Studies Francis, E., and B. Mayne. 1921. Experimental trans- on the immunofluorescent technique as a diag- mission of tularemia by flies of the species Chry- nostic tool in bacteriology. (Karlsson, ed., 1975) sops discalis. Pub. Hlth. Rpts. 36:1738-1746; also National Veterinary Institute, Stockliolm. 1922. Bull. 130:8-16. Hyg. Lab. Klock, L. E., p. F. Olsen, and T. Fukushima. 1973. L. p., B. 1962. review of Gebhart, and D. Thorpe. A Tularemia epidemic associated with the deer fly. tularemia (see USA-DPG). JAMA. 266:149-152. Green, R. G. 1943. Virulence of tularemia as related to Krinsky, W. L. 1976. Animal disease agents transmitted animal and arthropod hosts. Amer. Hyg. J. by horse flies and deer flies (Diptera: Tabanidae). 38:282-292. 13:225-275. J. Med. Ent. Green, R. G., C. L. Larson, F. Bell. 1939. Shock and J. Knudsen, a. B., D. M. Rees, and G. C. Collett. 1968. disease as the periodic of cause of the decimation Tularemia in Salt Lake County, Utah. p. 15-16. the snowshoe hare. Amer. Hyg. 30:83-102. J. In: Collett, G. C. and M. K. Benge, Eds. 21st Hesselbrock, W., and L. Foshay. 1945. The morpho- Ann. Mtg. Utah Mosq. Abmt. Assoc. Proc. (R. A. logy oi Bacterium tularense. Bact. 49:209-231. J. E. B.) 59:282. Hillman, C. and M. T. Morgan. 1937. Tularemia: C, Lane, R. S., and R. W. Emmons. 1977. Ecological and A report of a fulminant epidemic transmitted by epidemiological studies of tularemia in Califor- 108:538-540. the deerfly. JAMA. nia. Vector Views 24:39-49. H., A. Hoogstraal, with the editorial assistance of L. L., P. S. Nicholes. Lundgren, D. N. J. Marchette, and Gahin and a. Djigounian. 1970-72. Bibliogra- 1961. Certain immunological responses of wild phy of ticks and tickbome diseases. Special Pub- rodents and laboratory animals following chal- lication NAMRU 3, Cairo, Egypt. 4 Vols. lenge with Pasteurella tularensis (see USA-DPG HoPLA, C. E. 1974. 25-53. The Ecology of Tularemia, p. 1961). In: Brandley, C. A. and C. E. Cornelius, eds. Ad- 1962. The use of serologic and cutaneous allergic vances in veterinary science and comparative reactions in the diagnosis of tularemia in rodents Vol. medicine. 18. Academic Press, NY. and rabbits. Zoon. Rsch. 1:307-320. 120 Great Basin Naturalist Vol. 39, No. 2

Marchette, N. D. L. Lundgren, P. S. Nicholes, and J., Popek, K., E. Kopecna, N. Bieronska, Z. Cerny, B. E. D. Vest. 1961. Studies on infectious diseases in Janicek, and Z. Kozusnik. 1969. Epidemiolo- wild animals in Utah: Susceptibility of wild ani- gische Studie iiber das Vorkommen der Tula- mals to experimental tularemia. Zoon. Rsch. remic bei Arbeitern und Angestellten in Zuker- 1:49-73. fabriken im Siidmahrischen Raum. Zentralbl. P. S. Nicholes. 1961. Virulence Bakteriol. Parasitenkd. 210:502-517. Marchette, N. J. and and citrulline ureidase activity of Pasteiirella Quan, T. F. 1978. Pers. comm. Bact. 82:26-32. E., ed. et al. 1952. World atlas of epidem- tularensis. J. Rodenwaldt, diseases. In collaboration with R. E. Bader and 1974. Micro- ic Massey, E. D., and J. A. Mangiafico. others. Sponsorship: Bureau of Medicine and Sur- agglutination test for detecting and measuring se- gery. Navy Dept., Washington, D.C. Publisher: rum agglutinins of Francisella tularensis. Applied Falk, Hamburg. Microbiol. 27:25-27. RoDiANOvA, I. V. 1967. Respiration of the geographic va- Maximov, a. a. 1960. Natural tularemia foci in the rietfes of Pasteurella tularensis in the presence of USSR. Moscow and Leningrad. 290p. (In Rus- glycerine (Mammalia, man). Zh. Mikrobiol., Epi- sian). demiol., Immunobiol. 44:21-25 (Engl. Summ.).

disease of rodents. S., T. F. W. Anderson, H. M. McCoy, G. W. 1911. A plague-like Simmons, J. Whayne, G. Pub. Hlth. Bull. No. 43:53. HoRACK, and R. a. Thomas. 1944, 1951, 1954. McCoy, G. W., and C. W. Chapin. 1912. Bacterium Global epidemiology: a geography of disease and tularense, the cause of a plague-like disease of ro- sanitation. 3 vols. Lippincott, Philadelphia, Penn- dents. Pub. Hlth. Bull. No. 53:21. sylvania. Olsen, P. H. 1975. Tularemia, p. 191-233. In: Hubbert, Simpson, W. M. 1929. Tularemia: History, pathological W. T., W. F. McCulloch, and P. R. Schnurren- diagnosis, and treatment. Harper (Hoeber), New berger, eds. Diseases transmitted from animals to York. 139p. man. 6th ed. Charles C. Thomas, Springfield, Il- Skhodsky, E. 1966. Francisella tularensis culture on agar linois. peptone medium. Bull. Inst. Marine Medicine. Olsuf'yev, N. G. 1970. Taxonomy and characteristics of Gdansk 17:471-478.

the genus Francisella Dorofeev, 1947. J. Hyg., SoKAL, R. R. and F. G. Rohlf. 1969. Biometry. Freeman Epidemiol. Microbiol., Immunol. 14:67-76. & Co., San Francisco, California. Olsuf'yev, N. G., G. P. Rodnev, eds. 1960. Tula- 1974. Industrial, agricultural and mu- and Spendlove, J. C. remia. Publ. House Med. Lit., Moscow (parts nicipal microbial aerosol problems. Dev. in In- translated by U.S. Department of Commerce, dust. Microb. 15:20-27. Int. Publ. Rsch. Serv. No. 14105. 1956. 1962). Stagg, G. N., W. S. Tanner, and J. Lavender. Owen, C. R. 1970. Francisella infection, p. 469-483. In: Experimental infection of native animals with American Public Health Association diagnostic tularensis. Inf. Dis. 99:34-37. Pasteurella J.

procedures for bacterial, mycotic and parasitic Stoenner, H. G., R. Holdenried, D. Lackman, and J. infection. 5th ed. Amer. Pub. Hlth. Assn., New S. OsBORN, Jr. 1959. The occurrence of Coxiella York. burnetii. Brucella and other pathogens among the 1974. Genus Francisella p. 283-285. In: Buchan- fauna of the Great Salt Lake Desert in Utah. Am. an and Gibbons, eds., Burgey's manual of deter- Hyg. 8:590-596. J. Trop. Med. minative bacteriology. Waverly Press, Inc. Balti- Thorne, D. S. 1966. (see USA-DPG 1966a). more, Maryland 21202. Thorpe, B. D. 1965. Literature review and bibliography R., F. L. E. ar- Owen, C. J. Bell, W. Jellison, O. Buker, of Pasteurella tularensis in vertebrates and

and G. J. Moore. 1961. Lack of demonstrable en- thropods. 143p. (not published; typewritten copy hancement of virulence of Francisella tularensis with D. D. Parker). during animal passage. Zoon. Rsch. 1:75-85. Thorpe, B. D., and S. Marcus. 1962. Cellular aspects of Parker, D. D. 1957. Attempted transmission of P. tula- resistance in tularemia (abstract). Bact. Proc. fleas. rensis by three species of J. Econ. Ent. 62:78. 50:724-726. 1964a. Phagocytosis and intracellular fate of Pas-

Parker, D. D., and D. E. Johnson. 1957. Experimental teurella tularensis I. In vitro studies with rabbit transmission of Pasteurella tularensis flea Immunol. by the peritoneal noncellular phagocytes. J. Orchopeas Inf. Dis. leucopus Baker. J. 101:69-72. 92:657-663. Pearse, R. a. 1911. Insect bites. Northwest Med. 1964b. Comparison of two techniques to study in 3:81-82. vitro uptake and fate of Pasteurella tularensis. J. Philip, C. B. 1968. Overlap between Nearctic and Neo- Reticuloendothelial Soc. 1:418-422. tropical faunae of Tabanidae in western North 1965a. Phagocytosis and intracellular fate of Pas-

America (Diptera). Pan-Pac. Ent. 44:332-355. teurella tularensis II. In vitro studies with rabbit Philip, C. B., F. J. Bell, and C. L. Larsen. 1955. Evi- alveolar and guinea pig alveolar and perotoneal dence of infectious diseases parasites in Immunol. and a mononuclear phagocytes. J. peak population of blacktailed jackrabbits in Ne- 93:558-565. vada. Wildlife 19:225-233. J. Mgmt. 1965b. Phagocytosis and intracellular fate of Pas- PoLLiTZER, R. 1967. History and incidence of tularemia teurella tularensis III. In vivo studies with pas- in the Soviet Union. University, sera. Fordham Bronx, sively transferred cells and J. Immunol. New York. 366 p. 94:578-585. 1979 Stark: Review of Utah Tularemia 121

1965c. Passively transferred cells and sera in re- Rsch., Utah Univ. Contract DA-42-007-403- sistance to Pastettrella tularensis infections (ab- CML-427. Ecology & Epizoology Series No. 60, stract). Bact. Proc. 65:51. 66p. 1966. In vivo phagocytosis of Pasteurelh tula- 1962a. A review of tularemia. By L. P. Gebhardt, rensis (abstract). Bact. Proc. 66:67. and B. Thorpe. Prepared by Utah Univ. Contract 1967. Effects of streptomycin on intracellular DA-42-007-403-C M L-427(R). Pasteurella tularensis during in vitro phagocytic 1962b. Summary status report on Pasturella tula-

studies (abstract). Bact. Proc. (67: ). rensis. Prepared by Utah Univ., Special Report Thorpe, B. D., and R. W. Sidwell. 1962. Pathogenic No. 88u (R). organisms isolated from wild animals in western 1965. Special tularemia report. By D. D. Bode. Utah. Proc. Int. N. W. Conf. Dis. in Nature Prepared by Utah Univ., Ecology and Epizoology Comm. to Man 17:110-120. Series No. 93. Thorpe, B. D., R. W. Sidwell, and S. Marcus. 1964. 1966a. The persistence of Pasturella tularensis in Cellular aspects of resistance in Pasteurella in- soils of Dugway Proving Ground. By D. S. fections (abstract). Bact. Proc. 674:84. Thorne. DA Proj. No. 1B650212D624-04 USA Thorpe, B. D., R. W. Sidwell, D. E. Johnson, K. L. TECOM Proj. No. 5-7-9043-02. Smart, and D. D. Parker. 1965. Tularemia in 1966b. Protocol of operational procedures and the wildlife and livestock of the Great Salt Lake epizoological research. Prepared by Utah Univ. 1964. Contract DA-42-007-AMC-227(R). Utah Univ. Desert region, 1951 through Amer. J. Trop. Med. Hyg. 14:622-637. Series No. 134:42p. November 1966. U.S. Army Chemical Corps. 1958. Bibliography of tula- 1976. Ecology studies in the Bonneville Basin of remia. U.S. Army Chemical Corps, , west central Utah. Annual progress report for Maryland. 4th ed. 114p. 1973. DPG-FR-xlOOP. U.S. Army Deseret Test Center (USA-DTC). 1978. Environmental and ecology branch prog- 1971-1973. Ecology studies in western Utah. Pre- ress report for 1974 through 1976. Triennial Re- pared by EcoDynamics, Inc., , Salt port. DPG-TR-E-157A. Lake City, UT. Contract DAAD-09-70-C-0051. Vest, E. D., D. L. Lundgren, D. D. Parker, D. E. E. L. B. U.S. Army Dugway Proving Ground (USA-DPG). Johnson, Morse, J. Bushman, R. W. 1951-1969. A study of the ecology and epizool- Sidwell, and B. D. Thorpe. 1965. Results of a ogy of the native fauna of the Great Salt Lake five-year survey for certain enzootic diseases in of western Desert. Annual summary progress report. Pre- the fauna Utah. Amer. J. Trop. Med. pared by Utah Univ. Contracts DA-42-007-AMC- Hyg. 14:124-135. E. D., 35(R), DA-42-007-AMC-227(R), DA-18-064-CML- Vest, and N. J. Marchette. 1958. Transmission 2639, DA-42-007-403-CML-427, DAAD-09-69-C- of Pasteurella tularensis tularensis among desert 0030(R). rodents through infective carcasses. Science 1954. Ecology of disease transmission in native 128:363-364. animals. Prepared by Utah Univ. Contracts DA- Woodbury, A. M., ed. 1956. Ecological check list. The 18-108-CML-4776, DA-18-064-CML-2455, DA- Great Salt Lake Desert Series, Utah Univ., mim-

18-064-CML-3639(R). Semi-annual report. 1 June eographed report 125p. to 30 November 1954. 1964. Pathogen dissemination among biotic com- 1955. Ecology of tularemia transmission in native munities. Div. Biol. Sci. Misc. papers. Utah Univ. animals. Annual report 1954-1955. Contracts No. 4; also Bull. Utah Univ. 55(22): 1-282 (Tula- DA-18-064-CML-2639. Project Nos. 4-98-05-027. remia p. 209-218). 1961. Studies on the ecology and epizoology of Woodbury, A. M., and D. D. Parker. 1954. Studies of the native fauna of the Great Salt Lake Desert: tularemia, Pasteurella tularensis. Ecology of the certain immunological responses of wild rodents Great Salt Lake Desert. Ecol. Res., Utah Univ. and laboratory animals following challenge with Spec. Rpt. No. 2, 14p. Pasturella tularensis. Prepared by Inst. Env. Biol.