Volume 17, Number 1—January 2011
Reducing Baylisascaris procyonis Roundworm Larvae in Raccoon Latrines
Baylisascaris procyonis roundworms, a parasite of raccoons, can infect humans, sometimes fatally. Parasite eggs can remain viable in raccoon latrines for years. To develop a management technique for parasite eggs, we tested anthelmintic baiting. The prevalence of eggs decreased at latrines, and larval infections decreased among intermediate hosts, indicating that baiting is effective.
The emergence of zoonotic diseases, which account for ≈58% of all infectious diseases in humans, is linked to changing land use and resource consumption patterns (1). Ecosystem disturbances from human population growth and globalization result in rapid spread of zoonotic pathogens (2). Recent integrated approaches to solving global health issues acknowledge that wildlife reservoirs facilitate zoonotic pathogen emergence and emphasize the need for increased collaboration between the ecology and infectious disease communities (2). We describe a multidisciplinary collaboration that used an experimental approach to lower the prevalence, and possibly break the life cycle, of a zoonotic parasite, the Baylisascaris procyonis roundworm.
Raccoons (Procyon lotor) are the host of B. procyonis roundworms, intestinal parasites (3). Up to 82% of adult raccoons and 90% of juvenile raccoons are infected (3). Mature worms produce thousands of eggs daily (3). These eggs are eliminated through raccoon feces and accumulate at raccoon latrines (4). B. procyonis roundworm eggs remain infective for many years and can infect juvenile raccoons and intermediate hosts such as rodents and birds that ingest them (3). Transmission often occurs at raccoon latrines when eggs are ingested with seeds found in fecal material (4). Larvae migrate through intermediate host tissues and can enter the central nervous system, resulting in death (3). Adult raccoons become infected when they prey on infected intermediate hosts (3). Raccoon population densities have increased in response to increased anthropogenic resources that are available in agricultural and urban ecosystems (5). Thus, raccoon latrines often exist near human habitats, increasing the risk for zoonoses (4).
Reported cases of human B. procyonis roundworm infections are rare (n = 18), and all have occurred in North America; however, prevention is a public health priority because of the severity of the resulting neurologic disease (6–10). Our objective was to develop a management technique that could interrupt transmission of B. procyonis roundworm eggs between raccoons and intermediate hosts, ultimately decreasing the environmental levels of eggs and potential for reinfection. We examined the effects of latrine removal and treatment of raccoons by using randomly distributed anthelmintic baits on the basis of B. procyonis roundworm prevalence at latrines and among intermediate hosts. By implementing a specific, protocol-based approach to disease prevention, supported by experimentally derived data, we hope to provide public health officials with an effective, spatially explicit, prophylactic method for reducing infection risk.
We conducted this study in Grant, Miami, and Wabash counties in north-central Indiana in portions of the Upper Wabash Basin. This area is 88% agricultural; only 8% of the landscape remains forested (11). Some contiguous riparian forest remains; however, most patches are <5 hectares (ha; 1 ha = 10,000 m2) (11). Our experiment was conducted in 16 forest patches (1.91–8.80 ha). Eight treatment patches received anthelmintic baits, and 8 control patches did not. The range of patch sizes, levels of patch isolation, and raccoon densities in treatment and control patches were representative of the landscape (Figure).
In March 2007 (spring 07), we removed all visible latrines (n = 559) in the treatment patches. We located latrines by systematically searching all appropriate horizontal substrate and area at the bases of large trees throughout each forest patch (3). After manual removal, we used a torch to sterilize the substrate and surrounding soil associated with each latrine (Technical Appendix). At control sites, we sampled a minimum of 20 latrines (n = 198) by removing ≈2 g fecal material per fecal deposit at each latrine (12). We returned to our study sites 3 additional times for fecal sampling in October and November 2007 (fall 07), June 2008 (summer 08), and November 2008 (fall 08). During these subsequent visits, we sampled ≈2 g of fecal material per fecal deposit at a minimum of 20 latrines in all treatment and control patches. All samples were stored at −20°C until they were examined for B. procyonis roundworm eggs. Eggs were identified by microscopic examination following centrifugal fecal flotation in Sheather sugar solution (3). We identified B. procyonis roundworm eggs on the basis of size and morphologic appearance and designated each sample as positive or negative. Prevalence was measured as the proportion of positive samples at each study patch during each sampling period. Differences between pretreatment and posttreatment prevalence and between treatment and control patches were determined by using log linear analyses performed with PROC CATMOD SAS version 9.1 (SAS Institute Inc., Cary, NC, USA) (goodness-of-fit tests).
In spring 07, after the initial latrine removal from treatment patches, baits were distributed throughout treatment patches once a month for the duration of the study. Baiting densities were determined on the basis of average abundance of raccoons in each study patch (Technical Appendix).
Prevalence of B. procyonis roundworm larvae within an intermediate host, white-footed mice (Peromyscus leucopus), was determined. A minimum of 10 mice were captured from each of the 16 study patches during each of 3 sampling periods: 1 pretreatment (summer 07), and 2 posttreatment (fall 07 and summer 08). After capture, mice were euthanized with carbon dioxide and refrigerated until examination for B. procyonis roundworm larvae. Brains were removed and examined separately by pressing them between glass plates, and larvae were examined under a dissecting microscope. We recovered larvae from tissues digested in acid–pepsin solution (3). Larvae were counted and identified (3). Prevalence of infection was determined for mice within each study patch for each sampling period. Differences between treatment and control patches were determined by Fisher exact test (12).
We collected 1,797 fecal samples. Pretreatment sampling of latrines in spring 07 detected B. procyonis roundworm eggs at 757 (33%) of latrines sampled across all patches (Table). However, prevalence of eggs in treatment patches declined by >3-fold after baiting in all sampling periods (p<0.04). Our baseline pretreatment estimate of prevalence of infection among intermediate hosts did not differ (p = 0.426) between treatment patches (32%) and control patches (37%). Approximately 1 year after baiting activities began, we detected a significant decline in the prevalence of B. procyonis roundworm larvae in mice between treatment and control patches (27% vs. 38%; p = 0.05; Table).
Current public health initiatives to prevent human infections with B. procyonis roundworms focus on education of human health care and veterinary professionals (6). Our practical approach decreased prevalence of the parasite, suggesting decreased transmission and possibly reduced risk for humans. Baiting strategies have effectively controlled rabies (13) and decreased prevalence of zoonotic parasites, including Echinococcus multilocularis tapeworms (14). Our baiting strategy combined with latrine removal effectively decreased egg levels at latrines and ultimately decreased prevalence among mice. Hegglin and Deplazes (14) demonstrated a long-term decrease in prevalence of E. multilocularis tapeworms among foxes (definitive hosts) after monthly baiting for ≈4 years and conjectured that this decrease was caused by decreased infections among intermediate hosts. Our study supports their hypothesis because we measured decreases in prevalence among intermediate hosts after baiting. The reduction of prevalence at latrines and among intermediate hosts suggests that our low-cost approach (Technical Appendix) could have a lasting effect on transmission dynamics; however, further study to assess frequency of distribution and type and dose of baits for sustained prevalence is needed. Raccoon latrines are commonly found near homes (4), and implementation of baiting strategies, in conjunction with traditional raccoon management on public lands, could reduce the risk for transmission on nearby private properties.
Dr Page is an associate professor of biology at Wheaton College in Wheaton, Illinois. Her research interests include the transmission ecology of B. procyonis roundworms and the link between human land use and disease transmission.
We thank the landowners in Upper Wabash Basin who allowed us access to their properties. We are grateful for field and laboratory assistance provided by A. Beheler, G. Dharmarajan, P. Girgis, B. Griffin, R. Page, and W. Page. We also thank the 2 anonymous reviewers who provided helpful comments on the manuscript.
Financial support for this study was provided by Purdue University Center for the Environment at Discovery Park, the Wheaton College Alumni Association, the Aldeen fund, and the Science Division.
- Woolhouse ME, Gowtage-Sequeria S. Host range and emerging and reemerging pathogens. Emerg Infect Dis. 2005;11:1842–7.
- Kahn LH. Confronting zoonoses, linking human and veterinary medicine. Emerg Infect Dis. 2006;12:556–61.
- Kazacos KR. Baylisascaris procyonis and related species. In: Samuel WM, Pybus MJ, Kocan AA, editors. Parasitic diseases of wild mammals. Ames (IA): Iowa State University Press; 2001. p. 301–41.
- Page LK, Anchor C, Luy E, Kron S, Larson G, Madsen L, Backyard raccoon latrines and risk for Baylisascaris procyonis transmission to humans. Emerg Infect Dis. 2009;15:1530–1.
- Beasley JC, Rhodes OE Jr. Relationship between raccoon abundance and crop damage. Human-Wildlife Interactions. 2008;2:248–59 [cited 2010 Nov 29]. http://www.berrymaninstitute.org/journal/fall2008/Beasley_Rhodes.pdf
- Wise ME, Sorvillo FJ, Shafir SC, Ash LR, Berlin OG. Baylisascaris procyonis, the common roundworm of raccoons: a review of current literature. Microbes Infect. 2005;7:317–23.
- Chun CS, Kazacos KR, Glaser C, Bardo D, Dangoudoubiyam S, Nash R. Global neurological deficits with Baylisascaris encephalitis in a previously healthy teenager. Pediatr Infect Dis J. 2009;28:925–7.
- Hajek J, Yau Y, Kertes P, Soman T, Laughlin S, Kanani R, A child with raccoon roundworm meningoencephalitis: a pathogen emerging in your own backyard? Can J Infect Dis Med Microbiol. 2009;20:e177–80.
- Pai PJ, Blackburn BG, Kazacos KR, Warrier RP, Begue RE. Full recovery from Baylisascaris procyonis eosinophilic meningitis. Emerg Infect Dis. 2007;13:928–30.
- Perlman JE, Kazacos KR, Imperato GH, Desai RU, Schulman SK, Edwards J, Baylisascaris procyonis neural larva migrans in an infant in New York City. J Neuroparasitology. 2010;1:1–5 [cited 2010 Nov 29]. http://www.ashdin.com/journals/jnp/N100502.pdf
- Moore JE, Swihart RK. Modeling patch occupancy by forest rodents: incorporating detectability and spatial autocorrelation with hierarchically structured data. J Wildl Manage. 2005;69:933–49.
- Smyser TJ, Page LK, Rhodes OE Jr. Optimization of raccoon latrine surveys for quantifying exposure to Baylisascaris procyonis. J Wildl Dis. 2010;46:929–33.
- Sidwa TJ, Wilson PJ, Moore GM, Oertli EH, Hicks BN, Rohde RE, Evaluation of oral rabies vaccination programs for control of rabies epizootics in coyotes and gray foxes. J Am Vet Med Assoc. 2005;227:785–92.
- Hegglin D, Deplazes P. Control strategy for Echinococcus multilocularis. Emerg Infect Dis. 2008;14:1626–8.
Suggested citation for this article: Page LK, Beasley JC, Olson ZH, Smyser TJ, Downey M, Kellner KF, et al. Reducing Baylisascaris procyonis roundworm larvae in raccoon latrines. Emerg Infect Dis [serial on the Internet]. 2011 Jan [date cited]. http://dx.doi.org/10.3201/eid1701.100876