Wilderness and Environmental Medicine, 1, 1-8 (1996) ORIGINAL ARTICLE Blastomycosis in dogs: A fifteen-year survey in a very highly endemic area near Eagle River, Wisconsin, USA DENNIS 1. BAUMGARDNER, MD'*, NICK W. TURKAL, MD', and DANIEL P. PARETSKY, DVM2 IDepartment of Family Medicine, University ofwisconsin Medical School, Milwaukee, Wisconsin 53215, USA; 2Eagle River Animal Hospital, Eagle River, Wisconsin USA, Purpose: A recent study of blastomycosis in dogs has identified an area of high endemicity along waterways in North Central Wisconsin, USA, and suggested a bimodal age distribution of disease. The purpose of this study is to investigate the occurrence and features of dogs with blastomycosis over several years in this area. Methods: In June, 1994, a mail survey was sent to 216 owners of properties known to exist within the highly endemic area for blastomycosis west of Eagle River, Wisconsin. Owners were asked to list all dogs kept at that property since 1980, to detail their dogs' demographics and longevity and the occurrence of veterinarian-diagnosed blastomycosis. Features of dogs with and without disease were compared using Epi Info software. Results: Seventy-one (33%) of the surveys were returned, and 53 of these properties had housed one or more dogs during this time (87 total dogs). Seventeen (20%) of these dogs had a history of blastomycosis, and 28% of the 53 properties had housed one or more dogs with blastomycosis, All 17 dogs with blastomycosis lived on properties adjacent to or within 100 ft. of the shoreline compared to 76% of dogs without the disease (p = 0.03). Males and purebred dogs were not overrepresented in cases. Seventy-one percent of blastomycosis cases were three years of age or less at diagnosis (average age 3.0 years); 88% had been on the property three years or less until diagnosis, and 59% less than one year (average length 1.9 years). The average length of time on the property for dogs without blastomycosis was 5.7 years (age of 1eath, 12.4 years), indicating a significant difference between the two data groups. Conclusions: Among dogs in a highly endemic area, young age and recent exposure to the highly endemic parcel and very close proximity to a shoreline are risk factors for blastomycosis. Key words: blastomycosis, fungal disease, lung diseases, dog diseases Introduction Blastomycosis is a systemic and cutaneous fungal infection of humans, dogs and other domestic and wild animals that ranges in clinical presentation from asymptomatic to fulminant, lifethreatening illness. Primary infection in humans and dogs typically occurs following inhalation of Blastomyces dermatitidis spores from the environment and transformation to the yeast phase in the lungs. In humans, inapparent to severe acute or chronic pulmonary disease may result, * To whom all correspondence should be addressed. at: St. Luke's Family Practice Residency, 2901 W. Kinnickinnic River Parkway, Suite 175, Milwaukee, WI 53215, USA. 1080-6032 1996 Chapman & Hall
2 Baumgardner, Turkal and Paretsky Dissemination may occur and present as single or multiple lesions of the integument, skeletal system, genitourinary tract, central nervous system or other organs [1,2). In dogs, respiratory symptoms are also common presenting features, in addition to fever, anorexia, weight loss, lymphadenopathy, lameness and ocular disease (uncommon in humans). A variety of other organs may be involved [3). Blastomycosis is endemic in North America in the southeastern United States, the Great Lakes Region and the Mississippi and Ohio River Basins [1). It is frequently associated with outdoor activities in rural areas, including wilderness sites. As reviewed by DiSalvo [4], 10/11 outbreaks have occurred in rural areas in addition to two outbreaks on or near the site of the present report [5,6]. Implicated activities included camping, nature-walking, fishing and other forms of recreation. Blastomycosis in dogs is a harbinger of human disease, representing common-source environmental exposure rather than spreading between hosts [4). Evidence for this includes simultaneous outbreaks ofdisease in humans and dogs in the same area or household [5,7-9] and similar regions of high endemicity [7,10-14]. Vilas County, located in North Central Wisconsin, USA (46 N, 89-90 0 W), has the highest reported annual incidence of human blastomycosis. In the southeast corner, including the city of Eagle River, over 100 cases per 100,000 individuals occur each year [7]; the annual incidence is more than lo-fold higher in dogs [10]. This region has also been the site of two of the largest reported outbreaks of blastomycosis [5,6], which predominantly involved visitors to the area. Approximately 85% of the 867 square miles of Vilas County is forested, with most of the balance composed of glacially formed waterways (approximately 2300 miles of shoreline) and wetlands. The average elevation is approximately 1700 feet, the population density was 20 per square mile in 1990, and tourism is the major industry [15). Most county homesites are on or immediately adjacent to public or private forests representing a variety ofhabitats, most typically the mature upland mixeq forest [16]. Typical of such dwellings are those located just west of the city of Eagle River, near the confluence of the Eagle and Wisconsin Rivers at Watersmeet Lake. These sections are popular places for visitors and residents alike to recreate, as evidenced by several nearby seasonal dwellings, resorts and motels. This is due, in part, to the designation of Watersmeet Lake as a top-rated muskellunge fishing lake by the Wisconsin Department of Natural Resources. These sections also represent perhaps the most highly endemic area for blastomycosis ever reported [7,10]. The purpose of this report is to study the occurrence of blastomycosis in dogs in this area over several years in order to further quantify the extent of disease prevalence, and to investigate the bimodal age distribution previously observed for dogs with blastomycosis [10]. The latter may have implications regarding the acquisition of natural immunity to blastomycosis. Methods Plot registrations, including owner mailing addresses, were obtained from the Vilas County Records Department for the sections contiguous to the confluence of the Eagle and Wisconsin Rivers. In June, 1994, a single mail survey was sent to 216 owners of property along rural streets known to serve plots adjacent to the rivers or Watersmeet Lake (formed by the confluence). An unknown proportion of these properties represented unimproved lots or uninhabited dwellings. The survey instrument explained the purpose of the study and asked willing owners to indicate if they were year-round residents or visitors (including the months of usual habitation there) and to disclose their length of time at that address. They were asked to list all dogs kept at that site since 1980 (including dogs acquired there prior to 1980); the sex of each; the age at acquisition at that
Blastomycosis in Dogs 3 site; age at death, if appropriate; and whether or not the dog had ever been diagnosed with blastomycosis by a veterinarian. Surveys were collected by business reply mail. The chi-square test with Yates' correction or the Fisher exact test was used for analysis of the categorical data using Epi Info 5.01b software (Centers for Disease Control, Atlanta, GA, USA). The Wilcoxin two-sample test was used for continuous variables. Statistical significance was determined atp < 0.05. Results Seventy-one (33%) of the surveys were returned; 53 of these properties housed one or more dogs during this time, representing 87 total dogs. Seventeen (20%) of the dogs had a history of blastomycosis. At least one blastomycosis case was diagnosed every year between 1979-1993 except 1982, 1983, 1985, 1990 and 1991. Features of dogs with and without blastomycosis are presented in Table 1. The average age at diagnosis of blastomycosis was 3.0 years, and the age distribution is presented in Fig. 1. The average age at death for the 24 study dogs without blastomycosis that had died since 1980 was 12.4 years, a significant difference from the average age of blastomycosis diagnosis (p < 0.001). Ofthe 17 cases, 10 (59%) of the dogs died or were sacrificed due to blastomycosis, all at the same age as acquisition of disease. The remaining dogs survived with treatment: six were alive at the time of the survey (age range 1-11), and another left the property four years after diagnosis. The distribution of cases by length oftime at the present location prior to diagnosis is shown in Fig. 2. Fifty-nine percent of the dogs had been kept there less than one year (including the only seasonally present dog who had been on the property 7 consecutive months). The average length of time on the property before diagnosis of blastomycosis was 1.9 years. This differed significantly from the average length of time on the property for study dogs without blastomycosis (prior to June 1994 or at time of death or relocation) of 5.7 years (p < 0.001). One or more dogs with blastomycosis had been present in 15/53 (28%) of households. The average number of dogs per household did not differ between those households with and without blastomycosis (1.7 vs. 1.6). Among the 15 households reporting canine blastomycosis cases, the proportion of male dogs did not differ between blastomycosis cases and dogs without disease (l0/17 vs. 6/9;p > 0.05). The exact location of the homesite could be located for 52/53 respondent households (all 17 cases and 68170 dogs without blastomycosis). The geographic distribution of these 85 dogs with and without blastomycosis is shown in Fig. 3. All seventeen dogs with blastomycosis lived on properties situated 100 ft. or closer to the shoreline of the respective waterway compared to 52/68 Table 1. Comparison of dogs with and without blastomycosis: 1980 through June, 1994 Dogs with blastomycosis (n = 17) Dogs without blastomycosis (n = 70) p value Male Sex Purebred Seasonal Residence/Visitor* 10 (59%) 9 (53%) 1 (6%) 31 (44%) 47 (67%) 10 (14%) 0.42 0.42 0.28 *3 dogs without blastomycosis were weekend visitors; rest of seasonal dogs were present 6-9 consecutive warmer weather months per year.
4 Baumgardner, Turkal and Paretsky Number of Cases 6 5 4 3 2 1 0 0 1 2 3 4 5 6 7 Age At Diagnosis (Years) 8 9 10 Fig. 1. Distribution by age at diagnosis of 17 cases of blastomycosis: 1980-June, 1994. (76%) of dogs in Fig. 3 without blastomycosis (p = 0.03, 2-tailed Fisher exact test). This relationship remains statistically significant in the event that the two dogs not located for Fig. 3 also resided adjacent to the shoreline (p = 0.03). Properties housing dogs with blastomycosis were typified by mixed upland forestation [16] with a predominance ofred pine (Pinus resinosa), eastern white pine (Pinus strobus), balsam fir (Abies balsamea) and paper birch (Betula papyrifera); forested, sandy soil [17]; and abrupt, moderately steep, generally shaded shorelines. Discussion Still considered by many to be a relatively uncommon disease, blastomycosis is highly endemic in certain parts of the world [18]. It is a significant public health problem, particularly in the region in and near Eagle River, Wisconsin, where disease in dogs [10] is again a harbinger of human blastomycosis [7]. Among human residents of Vilas County with laboratory-confirmed blastomycosis between 1984 and 1990, 82% of cases occurred within the Eagle River area (annual incidence 101: 100,000), despite this area representing only 32% of the county population [7]. Dogs from a single veterinary practice in Eagle River between the years 1990-1993 had an estimated annual incidence of 1420:100,000 [10], and cases were concentrated near the city of Eagle River, including the area of the present report, as observed for endemic human cases [7]. Furthermore, of 31 humans who had contracted blastomycosis and kept dogs at their household ofexposure, 10 had reported veterinarian-diagnosed blastomycosis in one or more dogs [7]. The hyperendemicity ofthe confluence ofthe Eagle and Wisconsin Rivers at Watersmeet Lake is further substantiated by this report, which, within the limitations of this survey study, indicates a prevalence in dogs of 20%. One could suggest that our fairly low (33%) response rate (difficult to interpret due to an unknown quantity of unimproved lots being queried) might overestimate
Blastomycosis in Dogs 5 Number 01 Cases 12 10 B 6 4" 2 0 0 1 2 3 4 5 6 7 B 9 Length Of Time At Location (Years) 10 Fig. 2. Distribution of cases in Fig. 1 by length of time the dog had been on the present homesite prior to diagnosis. the prevalence due to a bias in the return of surveys (preferentially by owners of dogs with blastomycosis). Data from registries of two prior epidemiologic surveys in this area [7,10], however, reveal that, of 12 households with known blastomycosis queried in the present as well as previous studies, five did not respond to this particular survey. Nevertheless, within the highly endemic Vilas County area, this represents a smaller tract of very high disease prevalence, which additionally supports the hypothesis of microfoci of Blastomyces dermatitidis within areas of high endemicity [19], a concept first proposed for histoplasmosis [20]. Distinct microfoci have previously been identified in this area based on outbreaks involving a beaver lodge and dam [6] and an excavation site [5]. Residence within 1/4 mile (400 m) ofa waterway has been shown to be a significant risk factor for blastomycosis in dogs in the Vilas County area [10]. In the present report, all affected dogs were kept on properties adjacent to or within 100 ft. of the shoreline. This further implicates environmental factors present on the banks such as optimum soil type and ph, decaying vegetation, animal and bird droppings, abundant moisture and, perhaps, other unknown factors, all of which may be important components of the ecological niche of B. dermatitidis in this area. Banks of waterways are not the only niche for this fungus, however, as outbreaks of blastomycosis have occurred away from stream banks [4], as have soil isolations of B. dermatitidis [e.g. 21-23] and anecdotal cases in dogs never exposed to stream banks [24]. It is unclear whether or not shorelines are the primary reservoir of B. dermatitidis from which new, remote microfoci arise following airborne or fomite spread of the organism. The age distribution for blastomycosis in dogs in this small study was similar to that of the age-specific incidence rates in 59 dogs in the Vilas County region from 1990-1993 [10]. The
6 Baumgardner, Turkal and Paretsky o 00 o ~ooo ft~ fr N Fig. 3. Geographic distribution of 17 blastomycosis cases and 68/70 dogs without blastomycosis with identifiable homesites near Watersmeet Lake. Wisconsin. Each square C-) represents one blastomycosis case; each open circle CO) represents one dog without blastomycosis history. distribution of cases by length of time on the property in the present report suggests that the predominance of cases in younger dogs may be largely explained by a generally short exposure time (up to 3 years) needed for dogs to acquire the disease in this region. Dogs in this area without clinically apparent blastomycosis enjoy relative longevity. The 73 human blastomycosis cases from the Vilas County area were normally distributed with regard to age; however, half were visitors to the region or residents for three years or less [7]. The true proportion of mild or asymptomatic blastomycosis cases in humans and dogs [3] is not known. One might speculate from our data that naive hosts acquire B. dermatitidis within the first few years of exposure to a highly endemic area, that some proportion develop symptomatic disease, but that a larger proportion have insignificant disease and acquire natural immunity to the organism. Disease in older dogs may represent waning ofimmunity, as previously suggested [10], or chance avoidance for several years of specific microfoci. Presently, little is known about the acquisition of natural immunity to blastomycosis in dogs, and further studies are needed. It is postulated but not proven to occur in humans [25]. As briefly reviewed [10], some studies have suggestedthat male dogs may be more susceptible to blastomycosis than females. This study supports the findings of our previous report [10] that males are not overrepresented in areas of similar environmental exposure. Exposure factors seem to be more important than biological factors such as sex or breed.
Blastomycosis in Dogs 7 The microfocus ofblastomyces dermatitidis described in this report is in an area where people commonly choose to recreate or explore the outdoors. Exposure of a naive human or animal host to one of these regions may result in symptomatic blastomycosis. Return or travel to a non-endemic area may result in difficult diagnosis of this disease [26], as we observed from the registries of two of our prior reports [7,10]. Travelers must be aware ofthe risk of acquisition of blastomycosis and other systemic fungal disorders when traveling to a highly endemic area, and clinicians must have a high index of suspicion regarding these diseases when treating such individuals [11]. In summary, within the limitations of this study (33% survey response; an unknown percentage of queried uninhabited lots; and a current lack ofknowledge regarding environmental transmission of blastomycosis, subclinical cases and the presence and nature of acquired natural immunity), an area with 20% prevalence of blastomycosis in dogs has been identified. Young age, recent exposure (0-3 years) to the highly endemic parcel, and residence on property within 100 ft. of shoreline are risk factors for blastomycosis among dogs in this region. References I. AI-Doory, Y, DiSalvo, A.F., eds. Blastomycosis. New York: Plenum, 1992. 2. Bradsher, RW. Blastomycosis. Clin Infect Dis 1992; 14(Suppl. I), S82-S90. 3. Legendre, A.M. Blastomycosis in animals. In: AI-Doory, Y, DiSalvo, A.F., eds. Blastomycosis. New York: Plenum, 1992: 249-64. 4. DiSalvo, A.F. The epidemiology of blastomycosis. In: AI-Doory, Y, DiSalvo, A.F., eds. Blastomycosis. New York: Plenum, 1992: 75-104. 5. Baumgardner, D.I., Burdick, J.S. An outbreak ofhuman and canine blastomycosis. Rev Infect Dis 1991; 13, 898-905. 6. Klein, B.S., Vergeront, J.M., Weeks, R.I., et al. Isolation of Blastomyces dermatitides in soil associated with a large outbreak of blastomycosis in Wisconsin. New Engl J Med 1986; 314, 529-34. 7. Baumgardner, D.I., Buggy, B.P., Mattson, B.I., Burdick, J.S., Ludwig, D. Epidemiology of blastomycosis in a region of high endemicity in north central Wisconsin. Clin Infect Dis 1992; 15,629-35. 8. Armstrong, C.W., Jenkins, S.R, Kaufman, L., Kerkering, T.M., Rouse, B.S., Miller, G.B. Commonsource outbreak of blastomycosis in hunters and their dogs. J Infect Dis 1987; 155,568-70. 9. Sarosi, G.A., Eckman, M.R., Davies, S.F., Laskey, W.K. Canine blastomycosis as a harbinger of human disease. Ann Intern Med 1979; 91, 733-5. 10. Baumgardner, D.J., Paretsky, D.P., Yopp, A.C. The epidemiology of blastomycosis in dogs: north central Wisconsin, USA. J Med Vet Myco11995; 33,171-6. II. Proctor, M. Blastomycosis in Wisconsin. Wisconsin Epidemiology Bulletin 1995; 16(2): 1-5. 12. Archer, J.R., Trainer, D.O., Schell, R.F. Epidemiologic study of canine blastomycosis in Wisconsin. J Am Vet MedAssoc 1987; 190, 1292-5. 13. Furcolow, M.L., Chick, E.W., Busey, J.F., Menges, RW. Prevalence and incidence studies of human and canine blastomycosis. 1. Cases in the United States, 1885-1968. Am Rev Resp Dis 1970; 102,60-7. 14. Furcolow, M.L., Busey, J.F., Menges, RW., Chick, E.W. Prevalence and incidence studies of human and canine blastomycosis. II. Yearly incidence studies in three selected states, 1960-1967. Am J Epidemiol1970; 92,121-31. 15. Vilas county resource and conservation needs. Eagle River, Wisconsin: Vilas County Board of Supervisors, 1971. 16. Benyus, J.M. Northwoods Wildlife. Minocqua, Wisconsin: North Word Press, Inc., 1989. 17. Schulte, E.E.,Walsh, L.M. Management ofwisconsin Soils. 4th ed. Madison: University ofwisconsin Extension, 1993. 18. DiSalvo, A.F. The ecology of Blastomyces dermatitidis. In: AI-Doory, Y, DiSalvo, A.F., eds. Blastomycosis. New York: Plenum, 1992: 43-73.
8 Baumgardner, Turkal and Paretsky 19. Sarosi, G.A., Davies, S.P. Blastomycosis. Am Rev Respir Dis 1979; 120,911-38. 20. Campbell, C. The epidemiology of histoplasmosis. Ann Intern Med 1965; 62, 1333-6. 21. Sarosi, G.A., Serstock, D.S. Isolation ofblastomyces dermatitidis from pigeon manure. Am Rev Respir Dis 1976; 114, 1179-83. 22. Denton, J.P., DiSalvo, A.F. Additional isolations of Blastomyces dermatitidis from natural sites. Am J Trop Med Hyg 1979; 28, 697-700. 23. Bakerspigel, A., Kane, J., Schaus, D. Isolation of Blastomyces dermatitidis from an earthen floor in southwestern Ontario, Canada. J Clin Microbiol 1986; 24, 890-1. 24. Baumgardner, DJ., Paretsky, D.P. Practical field studies in family practice: blastomycosis. Wis Med J 1994; 93,117-8. 25. Klein, B.S. Immunology of blastomycosis. In: AI-Doory, Y., DiSalvo, A.F., eds. Blastomycosis. New York: Plenum, 1992: 133-63. 26. Lieberman, A. The case of the fumbled fungus. J Indiana State MedAssoc; 1963; 56,1017-22.