Blastomycosis in Urban Southeastern Wisconsin

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1 Blastomycosis in Urban Southeastern Wisconsin Melissa A. Lemke, MA; Dennis J. Baumgardner, MD; Charles F. Brummitt, MD; Geoffrey R. Swain, MD, MPH; Brian P. Buggy, MD; John J. Meidl, MD; Zachary J. Baeseman, BS; Andrea Schreiber, MA ABSTRACT Purpose: A previous study revealed a non-random distribution of blastomycosis cases by home site in urban Milwaukee County. This study was conducted to determine the proportion of cases with likely exposures solely in urban areas. Methods: Records of 68 urban southeastern Wisconsin individuals, including 45 residents of Milwaukee, 19 from suburban Milwaukee County, and 4 from outside Milwaukee County, diagnosed with blastomycosis between January 2002 and July 2007 were studied using medical record reviews, case reports, and telephone interviews. Geographic Information Systems (GIS) proximity analysis was then used to compare the distance between case and control home sites to environmental risk factors. Results: Of patients reporting their exposure history, 41 of 49 (84%) participated in outdoor work or leisure activities, and 12 of 47 (26%) engaged in fishing, hunting, camping, or hiking. Of the urban cases, 64 occurred among Milwaukee County residents; of those, 25 of 49 (51%) denied traveling, which suggests local urban exposure, and 8 of 11 (73%) specifically recalled urban waterway exposure prior to diagnosis. The 45 Milwaukee cases were concentrated on the north side of town and were closer to inland Author Affiliations: Center for Urban Population Health, Milwaukee, Wis (Lemke, Baumgardner, Swain, Schreiber); University of Wisconsin-Madison, School of Medicine and Public Health, Madison, Wis (Lemke, Brummitt, Buggy, Baeseman, Schreiber); Aurora UW Medical Group, Milwaukee, Wis (Baumgardner); Department of Family Medicine, University of Wisconsin-Madison, School of Medicine and Public Health, Madison, Wis (Baumgardner, Swain); Infectious Disease Associates, LLP, Milwaukee, Wis (Brummitt, Buggy, Meidl); City of Milwaukee Health Department, Milwaukee, Wis (Swain). Corresponding Author: Dennis J. Baumgardner, MD, Center for Urban Population Health, 1020 N 12th St, Ste 4180, Milwaukee, WI 53233; phone ; fax ; dennis.baumgardner@fammed.wisc.edu. waterways than a random sample of 6528 controls (median 690 versus 1170 meters; P=0.003), but not closer to parks. Conclusion: Southeastern Wisconsin residents may acquire blastomycosis solely in their local urban area, sometimes without specific outdoor exposures. Proximity to inland waterways is associated with blastomycosis cases in urban areas, similar to rural areas of Wisconsin. Clinicians should include blastomycosis in appropriate differential diagnoses of symptomatic individuals, even in urban residents without travel history or history of significant outdoor exposures. INTRODUCTION Blastomycosis is a potentially fatal systemic and cutaneous disease, endemic in Wisconsin, caused by the environmentally acquired dimorphic fungus Blastomyces dermatitidis. 1 The precise environmental niche of this fungus is unknown. 2 Case series and reports have suggested that humans and animals may acquire Blastomyces in urban areas of the upper Midwest. 3-6 A recent report revealed a non-random distribution of human blastomycosis cases in Milwaukee and an association with open urban watersheds; 7 however, this report and a case series from urban Rockford, Illinois 8 did not include patient interviews. Although the case rates for blastomycosis are much higher in some rural northern Wisconsin counties than in southeastern counties, low case rates in a very large urban population result in significant numbers of blastomycosis cases reported each year in patients from this region. The purpose of this report is to use an expanded case series to further characterize human blastomycosis in urban southeastern Wisconsin and to estimate what proportion of cases are acquired in this urban environment and what proportion of cases are acquired through travel to higher-prevalence areas of the state. 407

2 Table 1. Risk Factors Associated with Human Blastomycosis, Southeastern Wisconsin a Non-City of Milwaukee Milwaukee Total Residents (n=45) Residents (n=23) (n=68) GIS-determined Risk Factors Residence within 400 meters (.25 mile) 15/45 (33%) of park Residence within 400 meters (.25 mile) 13/45 (29%) of any waterway Self-reported Risk Factors Residence Near Waterway Near any waterway 10/31 (32%) 11/15 (73%) 21/46 (46%) Near lake 4/31 (13%) 6/15 (40%) 10/46 (28%) Near river 2/31 (6%) 2/15 (13%) 4/46 (7%) Near stream 4/31 (13%) 2/15 (13%) 6/46 (13%) Near wetland 0/31 (0%) 1/15 (7%) 1/46 (2%) Not near waterway 21/31 (68%) 4/15 (27%) 25/46 (54%) Any waterway exposure 11/15 (73%) 12/14 (86%) 23/29 (79%) Urban waterway exposure 8/10 (80%) 4/6 (67%) 12/16 (75%) among those without travel Forest exposure 4/6 (67%) 2/6 (33%) 6/12 (50%) Fishing, camping, hiking, hunting 8/32 (25%) 4/15 (27%) 12/47 (26%) Occupational exposure to soil 5/32 (16%) 1/14 (7%) 6/46 (13%) In-state travel 7/32 (22%) 6/15 (40%) 13/47 (28%) Out-of-state travel 8/33 (24%) 5/14 (36%) 13/47 (28%) All travel 13/33 (39%) 9/15 (60%) 22/48 (46%) Any risk factors b 26/33 (79%) 15/16 (94%) 41/49 (84%) a Denominator may vary as a result of missing data. b Risks include any self-reported travel, home site proximity to waterways, exposure to waterways, hunting/fishing/camping/hiking, forest exposure, farm exposure, occupational exposure to soil, home site proximity to excavation site, all-terrain vehicle use, and gardening/landscaping. METHODS This analysis is based on laboratory-confirmed blastomycosis cases (76% cases were confirmed by culture, with or without additional modalities; 10% by histopathology; 6% by fungal smear; and 8% by nucleic acid probe), with onset occurring between January 2002 and July 2007 in southeastern Wisconsin. Case reports were obtained from the City of Milwaukee Health Department s (Health Department) files of state-mandated reporting forms and were supplemented by a case registry from a large infectious diseases private practice located in Milwaukee. Of the case reports included in this study, all except 6 (1 Milwaukee, 1 suburban Milwaukee County, and all 4 non-milwaukee County cases) were captured by the Health Department reports. To maintain the consistency of the data across sites, researchers attempted to contact all patients identified via case reports, medical record reviews, or laboratory results for a follow-up telephone interview to supplement the data. Demographic, occupational, travel, and outdoor exposure data were collected from the medi- cal records and patient interviews using a standardized form that defined exposure period as 6 months to 3 weeks prior to the symptom onset date. Street addresses were geocoded and analyzed using ArcGIS software (ESRI, Redlands, CA), and distance to the nearest park, waterway, and inland waterway were calculated. Incidence rates by ZIP code tabulation areas (ZCTA) were calculated and mapped. Geographic, demographic, and interview data were analyzed using Minitab software (State College, PA). Categorical data was analyzed using Chi-square test with Yates correction for 2-by-2 tables or Fisher s exact test. The Kruskal- Wallis test was used to examine the differences between exposure risk factors based on gender. For Milwaukee cases, the Milwaukee Property File, a database of all residential home site addresses (139,216) was available. A control group was selected by randomly choosing 6528 of these home sites and geocoding them for comparison to the 45 Milwaukee cases that had geocoded addresses. Controls were determined using SPSS software to generate the random selection of home 408

sites. The number of controls was selected to afford 99.99% power to estimate an 11.5% frequency of distance within 400 meters (.25 mile) within 1.5 percentage points.

3 sites. The number of controls was selected to afford 99.99% power to estimate an 11.5% frequency of distance within 400 meters (.25 mile) within 1.5 percentage points. The Mann-Whitney test was used to compare the non-normally distributed, or outlier, distances between case and control home sites in relationship to waterways and parks. RESULTS During the study period, 75 southeastern Wisconsin blastomycosis cases were identified. Seven of these cases were among residents of non-urban areas and were excluded, leaving 68 urban cases (45 from the Milwaukee, 19 from suburban Milwaukee County, and 4 from non-milwaukee County addresses) as the focus of this study. The median age of these patients was 45 years (range years); 44% were black (Milwaukee is comprised of 39% black residents according to 2007 estimates), 42% were white, 7% were Hispanic; and (68%) were male. Of the study cases, 8% were reported in 2002, 13% in 2003, 19% in 2004, 20% in 2005, 19% in 2006, and 18% in 2007 (these percentages do not add up to 100% due to rounding). For the cases in which season of exposure could be determined, 16 occurred in winter (December-February), 15 in spring, 11 in summer, and 17 in fall (P=0.8). Pulmonary disease was the sole apparent manifestation in 51% of these cases, while 15% had extra-pulmonary disease only and 34% had both. Table 1 summarizes patient-reported risk factors. Denominators vary based on the number of patients interviewed by clinicians, Health Department staff or researchers who had specific recall available for that item. Specific exposure items were not available for some subjects. Three risk factors were reported most frequently: engaging in travel (22 of 48 or 46% of patients interviewed), home site near a waterway (21 of 46, or 46%), and exposure to any waterway (23 of 29, or 79%). Of residents in Milwaukee County and the cities of Kenosha, Racine, and Waukesha, 26 of 48 (54%) denied travel outside of their metropolitan area of residence. Overall risk factors in this study did not differ significantly by gender (data not shown); however, comparison numbers were low. Of Milwaukee County cases, 19 of 44 (43%) cases reported travel outside of the metropolitan area where they reside, and 19 of 43 (45%) reported living on or near waterways. In Milwaukee County, where we had both Health Department mandatory reports and private practice case findings, we estimate the minimum annual incidence rate of symptomatic cases to be 1.2/100,000. Figure 1. Milwaukee County blastomycosis incidence, January 2002 through July Milwaukee cases display a similar exposure pattern. Of these cases, 13 of 33 (39%) reported travel and 10 of 31 (32%) reported living on or near waterways. However, according to GIS analysis, 13 of 45 (29%) lived within 400 meters of a waterway and 15 of 45 (33%) lived within 400 meters of a park. Figure 1 depicts the distribution of blastomycosis in Milwaukee County by the ZIP code tabulation area associated with the patient s residence. (Individual locations are not indicated to protect patient privacy). In Milwaukee, the highest case incidence is on the near-north side. Participants were asked to share their occupational histories and information about their leisure activities, including fishing, hiking, camping, hunting, landscaping, and all-terrain vehicle use. Only a minority of patients reported these potential risk factors (Table 1). The fishing, hunting, camping, or hiking category was the most commonly reported (26%). GIS analysis of the 45 Milwaukee cases indicated that case home sites were closer to inland waterways than control home sites (median 690 versus

4 meters, P<0.001). Similarly, cases were more likely than controls to live within 400 meters of an inland waterway other than Lake Michigan (29% versus 15%, P=0.019). However, when Lake Michigan was included, these differences were no longer statistically significant (640 versus 870 meters, P=0.066; and 29% versus 21% for within 400 meters, P=0.249). Case and control home sites were similar median distances from the nearest park (510 versus 480 meters; P=0.49). DISCUSSION Our Milwaukee County case series suggests that urban geography, specifically the presence of open urban watersheds, could increase the likelihood of contracting blastomycosis. 7 The current study ( ) includes data regarding travel, outdoor work, and leisure activities. Limitations include the retrospective nature of the study, incomplete recollection by subjects, and incomplete data on subjects who were unavailable for follow-up interviews. Nearly half of the urban residents queried did not report travel outside of their immediate metropolitan area, suggesting that blastomycosis was acquired in the patients own urban environment. A majority of these urban residents, however, have reported some potential outdoor risk factors within their urban environment such as exposure to waterways, forests, or hunting/fishing/camping/hiking. Eight cases lacked significant outdoor risk-factor exposure, which is consistent with reports of a small number of domestic animal cases that also lacked significant outdoor exposure. 3,6 Our study suggests that living in a home near a waterway may be an important general risk factor for blastomycosis, corroborating findings from rural Wisconsin While consistent in rural and urban studies, the mechanism of the association of blastomycosis case home sites and nearby waterways is unclear. A majority of queried patients recalled waterway exposure, a self-reported measure that may have included recreation near urban waterways or residence on them. This exposure may have led to direct contact with Blastomyces microenvironments along stream banks Alternatively, animals or other vectors may bring the organism to Blastomyces-hospitable microenvironments near homes. 6,13 further evidence that blastomycosis is endemic in both urban and rural areas. The substantial proportion of Milwaukee County cases that did not report travel further suggests that blastomycosis is endemic to this county. Therefore, clinicians should include blastomycosis in appropriate differential diagnoses of symptomatic individuals, even for urban residents without travel history or significant outdoor exposures. Acknowledgments: The authors would like to acknowledge Angie Hagy, Jill LeStarge, Sandy Coffaro (City of Milwaukee Health Department), Carol Krey (Infectious Disease Associates), and Daniel Long (Aurora Health Care) for their assistance with this study. Funding/Support: None declared. Financial Disclosures: None declared. References 1. Chapman SW. Blastomyces dermatitidis. In: Mandell GL, Bennett JE, Dolin R, eds. Principles and Practice of Infectious Diseases. 5th ed. Philadelphia, PA: Churchill Livingstone; 2000: Restrepo A, Baumgardner DJ, Bagagli E, et al. Clues to the presence of pathogenic fungi in certain environments. Med Mycol. 2000;38(Suppl 1): Baumgardner DJ, Paretsky DP. Blastomycosis: more evidence for exposure near one s domicile. WMJ. 2001;100(7): Kitchen MS, Reiber CD, Eastin GB. An urban epidemic of North American blastomycosis. Am Rev Respir Dis. 1977;115: Lee D, Eapren S, VanBuren J, Jones P, Baumgardner DJ. A young man who could not walk. WMJ. 2006;105(1): Blondin N, Baumgardner DJ, Moore GE, Glickman LT. Blastomycosis in indoor cats: suburban Chicago, Illinois, USA. Mycopathologia. 2007;163: Baumgardner DJ, Knavel EM, Steber D, Swain GR. Geographic distribution of human blastomycosis cases in Milwaukee, Wisconsin, USA: association with urban watersheds. Mycopathologia. 2006;161: Manetti AC. Hyperendemic urban blastomycosis. Am J Public Health. 1991;81: Archer JR, Trainer DO, Schell RF. Epidemiologic study of canine blastomycosis in Wisconsin. J Am Vet Med Assoc. 1987;190: Baumgardner DJ, Paretsky DP, Yopp AC. The epidemiology of blastomycosis in dogs: north central Wisconsin, USA. J Med Vet Mycol. 1995;33: Klein BS, Vergeront JM, Weeks RJ, et al. Isolation of Blastomyces dermatitidis in soil associated with a large outbreak of blastomycosis in Wisconsin. N Engl J Med. 1986;314: Klein BS, Vergeront JM, DiSalvo AF, Kaufman L, Davis JP. Two outbreaks of blastomycosis along rivers in Wisconsin. Am Rev Respir Dis. 1987;136: Baumgardner DJ. Microecology of Blastomyces dermatitidis: the ammonia hypothesis. Med Mycol. 2009;In Press. CONCLUSION Blastomycosis has long been considered endemic to rural Midwestern areas. While further case series of urban blastomycosis are needed, this study provides 410

5 The mission of the Wisconsin Medical Journal is to provide a vehicle for professional communication and continuing education of Wisconsin physicians. The Wisconsin Medical Journal (ISSN ) is the official publication of the Wisconsin Medical Society and is devoted to the interests of the medical profession and health care in Wisconsin. The managing editor is responsible for overseeing the production, business operation and contents of Wisconsin Medical Journal. The editorial board, chaired by the medical editor, solicits and peer reviews all scientific articles; it does not screen public health, socioeconomic or organizational articles. Although letters to the editor are reviewed by the medical editor, all signed expressions of opinion belong to the author(s) for which neither the Wisconsin Medical Journal nor the Society take responsibility. The Wisconsin Medical Journal is indexed in Index Medicus, Hospital Literature Index and Cambridge Scientific Abstracts. For reprints of this article, contact the Wisconsin Medical Journal at or wmj@wismed.org Wisconsin Medical Society

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