Characterization of environmental sources of the human and animal pathogen Cryptococcus gattii in British Columbia, Canada, and the Pacific Northwest of the United States

Abstract

Cryptococcus gattii has recently emerged as a primary pathogen of humans and wild and domesticated animals in British Columbia, particularly on Vancouver Island. C. gattii infections are typically infections of the pulmonary and/or the central nervous system, and the incidence of infection in British Columbia is currently the highest reported globally. Prior to this emergence, the environmental distribution of and the extent of colonization by C. gattii in British Columbia were unknown. We characterized the environmental sources and potential determinants of colonization in British Columbia. C. gattii was isolated from tree surfaces, soil, air, freshwater, and seawater, and no seasonal prevalence was observed. The C. gattii concentrations in air samples were significantly higher during the warm, dry summer months, although potentially infectious propagules (<3.3 microm in diameter) were present throughout the year. Positive samples were obtained from many different areas of British Columbia, and some locations were colonization "hot spots." C. gattii was generally isolated from acidic soil, and geographic differences in soil pH may influence the extent of colonization. C. gattii soil colonization also was associated with low moisture and low organic carbon contents. Most of the C. gattii isolates recovered belonged to the VGIIa genetic subtype; however, sympatric colonization by the VGIIb strain was observed at most locations. At one sampling site, VGIIa, VGIIb, VGI, and the Cryptococcus neoformans serotype AD hybrid all were coisolated. Our findings indicate extensive colonization by C. gattii within British Columbia and highlight an expansion of the ecological niche of this pathogen.

FIG. 1.

Overview of geographic zones designated according to the NTS and the USGS in which environmental sampling was conducted. Sampling grid regions 44123-A1B4, 45122-C1D4, and 45122-C5D8, located in the state of Oregon, are beyond the extent of this map.

FIG. 2.

Map of Vancouver Island, the Gulf Islands, the lower mainland of British Columbia, and northern Washington state, showing the distribution of reported human and animal cases up to December 2005 as well as that of sampling sites from which positive and nonpositive environmental samples were obtained between October 2002 and January 2006.

FIG. 3.

Distribution of environmental sampling sites within a provincial park in geographic zone 092F/08. Positive samples were typically obtained from areas with relatively low tree densities, e.g., along the entrance road, around parking lots, and in the beach area.

FIG. 4.

Properties of soil samples colonized by C. gattii. Concentrations of C. gattii are expressed with respect to the dry weight of the soil.

FIG. 5.

Survival of a British Columbian C. gattii VGII isolate over 1 year in distilled water at room temperature (▵) and 4°C (▴), ocean water at room temperature (⋄) and 4°C (♦), filter-sterilized ocean water at room temperature (□) and 4°C (▪), 10% NaCl at room temperature (⋆) and 4°C (★), 15% NaCl at room temperature (○) and 4°C (•), and 20% NaCl at room temperature (▿) and 4°C (▾).

FIG. 6.

Characterization of air samples collected systematically between 2002 and 2004. (A) Mean C. gattii concentrations among all air samples (closed squares; n = 310) and positive air samples (open squares; n = 82) collected at different months of the year. (B) Mean concentrations of C. gattii stratified by propagule size during different months of the year. Andersen air samples were collected from February through October, for which the C. gattii concentrations shown represent those among all attempted samples (n = 118). (C) Mean C. gattii concentrations detected in air samples collected from different geographic grid regions of British Columbia.