Abstract
The raccoon (Procyon lotor) is an omnivorous mammal that is widely distributed throughout North America.8 The raccoon has adapted well to both urban and rural environments with populations increasing in both areas.6 This generates greater contact opportunity between people and raccoons and creates potential for human and animal exposure to parasites normally harbored by these animals. One of the intestinal parasites, Baylisascaris procyonis, has been associated with fatalities in both humans and animal species.1,5,7,11,12,23 This parasite has a predilection for the central nervous tissue in aberrant hosts and has been reported as the cause of ocular, cerebrospinal, and visceral larval migrans in humans, avian, and other mammalian species.5,9-11
Introduction
In this study, prevalence patterns of patent Baylisascaris procyonis infections were examined in raccoons from a state park (Siloam Springs State Park, Adams County, Mt. Sterling, IL, USA) and a surrounding rural area (Adams County) in west-central Illinois. Differences in fecal shedding among raccoons by age, sex, geographic, and seasonal profiles were examined to provide more information on the epidemiology of this disease.
Methods
The study was conducted from September 1989 to October 1993 with trapping seasons divided into fall (August–October) and spring (March–June). Following live capture, raccoons were sedated with Telazol® (Tiletamine HCl and Zolazepam HCl; Fort Dodge Laboratories, Inc., Fort Dodge, IA, USA) at 5 mg/kg i.m. and fecal samples were collected rectally. Fecal material was stored in a 2.5% potassium dichromate solution until submitted to the University of Illinois (College of Veterinary Medicine, Urbana, IL, USA) for parasitologic testing.
Age was estimated in the field by evaluation of facial and body features, tooth eruption, and body weight.15 Raccoons were categorized as juveniles, yearlings, or adults. Juveniles were classified as animals born in the spring or entering their first fall for the current trapping year while yearlings were those in the subsequent spring and fall seasons. Adults were classified as animals past the second spring following birth. A first premolar was extracted from yearling and adult animals to confirm the age by evaluating the cementum annuli.6
To evaluate for eggs, fecal material was centrifuged (1,500 g for 5 min) and the fecal pellet resuspended in Sheather’s sugar solution. A coverslip was placed on the tube, and the sample was centrifuged (1,200 g for 10 min) a second time. The coverslip was placed on a slide and reviewed under light microscopy at 100–450x. The mean dimensions of the B. procyonis egg was 68×55 µm. The eggs were golden-brown, ellipsoidal, and had a granular texture.
Risk factors were screened at the univariate level and then compared, simultaneously, using logistic regression (SAS). Analyses were conducted using SAS with p<0.05 considered to be statistically different.19,20
Results
Of 392 animals tested, 149 (38%) were found to be actively shedding B. procyonis. Juvenile raccoons were more likely have a patent infection (70%) than yearlings (31%) or adults (28%). Male raccoons were more likely have a patent infection (45%) than were females (30%). Raccoons captured in the park were less likely to have a patent infection (26%) than those in the rural area (46%). Raccoons captured during the spring season were less likely to be shedding eggs (34%) than those captured in the fall (41%). However, when juveniles were excluded from the comparison, because there were no samples collected from this age group in the spring, shedding of B. procyonis was lower in the fall (23%) than the spring (34%).
Discussion
Baylisascaris procyonis is the common roundworm of raccoons.19 Previous studies have reported prevalence of B. procyonis in raccoons from 7.5–82.0%.2,4,11,13,16,18 These reports were of adult worms diagnosed at necropsy except two reports which were from fecal samples with prevalence of 20.3 and 73%.13,18 The prevalence of egg shedding in this study (38%) is within the range but probably underestimates the true infection rate. Negative fecal samples are often the result of occult infections, which are not considered detrimental to aberrant hosts. Although active parasite burdens may not always be represented by evaluating fecal samples, prevalence of egg shedding is a measure of transmission and zoonotic potential. Characterization of age, gender, site, and seasonal trends are important in determining when the risk of exposure is greatest.
In this study, egg shedding was significantly higher in juveniles, relative to yearlings and adults. Juveniles become infected after ingesting infective eggs, infective intermediate hosts, and possibly through direct infection from their dams through the placenta or mammary secretions.11,13,18 Adult raccoons become infected predominantly by ingestion of infective intermediate hosts.11
Egg shedding in males was significantly higher than in females. It has been speculated that prevalence was lower in females due to transplacental and transmammary migration of larvae from females to juveniles thereby decreasing the developing number of mature adults.
Egg shedding was more likely in the rural area than the park area. Raccoons often use a latrine for defecation.3,23 There was less topographic relief in the rural area than park area. It has been reported that higher numbers of B. procyonis infections occur in areas with little topographic relief.4,19 Differences in habitat and other environmental influences could affect the social behavior and defecation site selection of raccoons. Further research is needed to explore ecologic mechanisms responsible for this difference.
It was reported that 80% of the B. procyonis detected in raccoons from New York were collected in the fall with the overall prevalence (for the fall) at 42.4%; this was nearly identical to the current study findings (41%).13 The higher fall prevalence in the present study was due to the number of juveniles captured. Among yearlings and adults, fewer were shedding B. procyonis in fall than spring. The primary diet of raccoons in the spring is from animal sources.8 The pre-patent period for B. procyonis is 30–35 days.11 This provides adequate time for raccoons to develop higher rates of infection during the spring sampling season. Yearling and adult raccoons are more likely to feed on plant material during the fall, which might also account for the lower prevalence identified in these animals. The lower prevalence of egg shedding in adults during the fall also supports previous reports of self-clearance in the fall and possible resistance to subsequent infections.13 The prevalence of egg shedding was lower in the fall than the spring in adult females; however, the difference was insignificant. This lower prevalence in the fall does support a role for transmammary larval transmission as parturition often starts in April, however it is variable.14 Further research is needed to determine if transmammary transmission does occur or if other factors, such as immunologic or dietary habits, may also play a role.
The findings of this study indicate the importance of preventative measures for individuals working with and around raccoons. The high prevalence of B. procyonis in juvenile raccoons poses a special threat to those who work closely with them, such as wildlife rehabilitators or pet owners. Children playing in sandboxes, on fallen logs, or areas where raccoons have established latrines are also at risk of exposure to potentially infectious larvae. Persons utilizing recreational facilities should also practice strict hygiene around areas potentially contaminated by raccoons. Bleach can be used to treat areas used by raccoons, although only fire destroys B. procyonis.11 Feeding of raccoons, which can concentrate them in large numbers, should be discouraged in both public and private settings. Raccoons in rehabilitation facilities or zoological parks should be quarantined from other species to decrease the risk of contamination.
Acknowledgments
This project was supported by the Illinois Natural History Survey with funds made available through Federal Aid for Wildlife, project number W-104-R-4.
†This study is pending publication in the Journal of Zoo and Wildlife Medicine.
Literature Cited
1. Armstrong D.L., R.J. Montali, A.R. Doster, and K.R. Kazacos. 1989. Cerebrospinal nematodiasis in macaws due to Baylisascaris procyonis. J ZooWildl Med. 20: 354–359.
2. Bafundo K.W., W.E. Wilhelm, and M.L. Kennedy. 1980. Geographic variation in helminth parasites from the digestive tract of Tennessee raccoons. J Parasitol. 66: 134–139.
3. Caldwell J. A. 1963. An investigation of raccoons in north-central Florida. M.S. Thesis University of Florida. 107.
4. Cole R.A. and W.L. Shoop. 1987. Helminths of the raccoon in western Kentucky. J Parasitol. 73: 762–768.
5. Fox A.S., K.R. Kazacos, N.S. Gould, P.T. Heydemann, C. Thomas, and K.M. Boyer. 1985. Fatal eosinophilic meningoencephalitis and visceral larva migrans caused by the raccoon ascarid. New Engl J Med. 312 : 1619–1623.
6. Grau G.A., G. C. Sanderson, and J. P. Rogers. 1970. Age determination of raccoons. J Wildl Mgmt. 43:364-372.
7. Hoffman C.O. and J.L. Gottschang. 1977. Numbers, distribution, and movements of a raccoon population in a suburban residential community. J Mammol. 58: 623–636.
8. Kaufman J.H. 1982. Raccoon and Allies. In: Wild Mammals of North America. 1st ed. Baltimore, Maryland, Johns Hopkins University Press.
9. Kazacos K.R. 1983. Raccoon roundworms. A cause of animal and human disease. Bulletin No. 422. West Lafayette, Indiana. Purdue University Agricultural Experiment Station, 1–25.
10. Kazacos K.R. and E.A. Kazacos. 1984. Experimental infection of domestic swine with Baylisascaris procyonis from raccoons. Amer J of Vet Res. 45: 1114–1121.
11. Kazacos K.R. and W.M. Boyce. 1989. Baylisascaris larva migrans. J Amer Vet Med Assoc. 195: 894–903.
12. Kazacos K.R., S.D. Fitzgerald, and W.M. Reed. 1991. Baylisascaris procyonis as a cause of cerebrospinal nematodiasis in ratites. J Zoo and Wildl Med. 22: 460-465.
13. Kidder J.D., S.E. Wade, M.E. Richmond, and S.J. Schwager. 1989. Prevalence of patent Baylisascaris procyonis infection in raccoons in Ithaca, New York. J Parasitol. 75: 870–874.
14. Lehman L.E. 1968. September birth of raccoons in Indiana. J Mammol. 49 126–127.
15. Nixon C.M., J.B. Sullivan, R. Koerkenmeier, A.A. Rothering, J. Thomas, J. Stevens, L.L. Hungerford, M.A. Mitchell, G.F. Hubert, and R. D. Bluett. 1994. Illinois raccoon investigations. Illinois Natural History Survey, Fed. Aid in Wildlife Restoration Project Report, W-104-R-5. 219.
16. Schaffer G.D., W.R. Davidson, V.F. Nettles, and E.A. Rollor. 1981. Helminth parasites of translocated raccoons in the southeastern United States. J Wildl Dis. 17: 217–226.
17. Shoop W.L. and K.C. Corkum. 1987. Maternal transmission by Alaria marcianae and the concept of amphiparatensis. J Parasitol. 73: 110–115.
18. Snyder D.E. and P.R. Fitzgerald. 1985. The relationship of Baylisascaris procyonis to Illinois raccoons (Procyon lotor). J Parasitol. 71: 596–598.
19. Snyder D.E. and P.R. Fitzgerald. 1987. Contaminative potential, egg prevalence, and intensity of Baylisascaris procyonis-infected raccoons from Illinois, with a comparison of worm intensity. Proc Helminthological Soc of Washington. 54: 141–145.
20. Sprent J.F.A. 1955. On the invasion of the central nervous system by nematodes. II. Invasion of the nervous in ascariasis. Parasitol. 45: 41–55.
21. Statistical Analyses Systems (SAS) Institute Incorporated. 1989. SAS/STAT Users Guide, ver 6. 4th ed., vol 1. Cary, North Carolina, SAS Institute Incorporated. 851–889.
22. Statistical Analyses Systems (SAS) Institute Incorporated. 1989. SAS/STAT Users Guide, ver 6. 4th ed., vol 2. Cary, North Carolina, SAS Institute Incorporated. 1071–1126.
23. Tester J.R. 1953. Fall food habits of the raccoon in the South Platte Valley of northeastern Colorado. J Mammol. 34: 500–502.