Epizootiology of an outbreak of cerebrospinal nematodiasis in cottontail rabbits and woodchucks

An epizootic of cerebrospinal nematodiasis in cottontail rabbits (Sylvilagus floridanus) and woodchucks (Marmota monax) caused by Baylisascaris procyonis larvae followed the establishment of an ascarid-infected raccoon (Procyon lotor) population in a woodlot. Five of seven raccoons examined from the woodlot harbored ascarids, with one heavily infected animal shedding approximately 27,500 eggs per gram of feces. A laboratory-reared cottontail rabbit developed neurologic disease due to larval migration 80 days after infection with B. procyonis eggs from the raccoons.     

Survey of raccoons on Key Largo, Florida, USA, for Baylisascaris procyonis

Numbers of the endangered Key Largo woodrat (KLWR; Neotoma floridana smalli) have been declining for at least 25 yr. The raccoon (Procyon lotor) roundworm, Baylisascaris procyonis, has been found to have an adverse effect on the survival of Alleghany woodrats (N. magister). High densities of raccoons can exacerbate this problem by increasing the amount of feces containing viable eggs of B. procyonis available to woodrats. In 2002, 64 fecal samples were collected and examined for eggs of B. procyonis from >32 raccoons within the KLWR's known range on Key Largo, Florida, USA. All samples were negative for eggs of B. procyonis. Raccoon density in this area was approximately 0.62 raccoons/ha. Despite this high density of raccoons, B. procyonis does not appear to be a threat to the KLWR population.     

Distribution, prevalence, and genetic characterization of Baylisascaris procyonis in selected areas of Georgia

Baylisascaris procyonis is an intestinal nematode of raccoons (Procyon lotor) that can cause fatal larval migrans in numerous species of birds and mammals, including humans. Although this parasite has historically been absent in the southeastern United States, it has been found in isolated regions in the Appalachian Mountains and was recently documented in DeKalb County, Georgia. The first objective of the current study was to investigate the distribution and prevalence of B. procyonis in selected populations of raccoons in Georgia. Intestinal tracts of 312 raccoons from 25 Georgia counties were examined for B. procyonis. The only county where B. procyonis was detected was Clarke County, where 12 of 116 (10.3%) raccoons were infected. In Clarke County, significantly more juveniles (P = 0.049) were infected compared with adults, and no differences in prevalence were noted by sex, season of capture, or land use (rural vs. urban); however, significantly (P = 0.0370) higher worm burdens were found in infected raccoons from urban/suburban locations compared with rural areas. In addition, Toxascaris leonina , a morphologically similar ascarid, was found in 3 raccoons from Clarke County (n = 2) and Morgan County (n = 1). A second objective was to determine if sequence polymorphisms were associated with B. procyonis from different geographic regions. Because sequences from a single worm from Japan had been entered into GenBank, we obtained nematodes from Kentucky and Texas for comparison with our samples from Georgia. Sequence analysis of the 18S and 5.8S rRNA genes and the internal transcribed spacer (ITS) -1 and ITS-2 regions confirmed Georgia samples were B. procyonis. Although several polymorphic bases were observed within both ITS regions, none was associated with a particular geographic location. These data indicate that the distribution of B. procyonis within Georgia is increasing and only limited genetic variation is present in the rRNA and ITS gene regions among B. procyonis from the southern United States and introduced populations in Japan.     

Frequency of deposition and location of Baylisascaris procyonis eggs in raccoon feces

Baylisascaris procyonis is a large ascarid nematode found in the small intestine of raccoons (Procyon lotor). Infection with larvae of B. procyonis can produce visceral, ocular, and neural larval migrans in humans. Infected raccoons can shed millions of eggs a day in their feces. However, it is unknown whether eggs are consistently shed or whether eggs occur at irregular intervals by the population of female nematodes within a host. We trapped, infected, and collected daily fecal samples from 11 raccoons maintained in captivity. Eggs from B. procyonis were obtained from anterior, central, and posterior sections of raccoon feces, isolated by flotation, and quantified under 100× magnification. Naturally infected raccoons were collected and used as a comparison with the experimentally infected group. All raccoons in the experimental group (n=11) became infected with B. procyonis after consuming one infected mouse. Additionally, differential egg deposition rates were observed among individual raccoons from the experimental and naturally infected groups. Mean number of eggs per gram of feces (means±SE) was 16,563±4,321, which was less than previously reported for the species. However, no differences (F(2,30)=0.84, P=0.45) were noted in mean number of eggs per gram of feces among fecal sections. Wildlife biologists, veterinarians, health officials, and researchers of B. procyonis should collect daily fecal samples for a minimum of 3 days before identifying a raccoon as negative for B. procyonis infection. However, it does not matter where within the fecal matter the sample is obtained.     

Land-use effects on prevalence of raccoon roundworm (Baylisascaris procyonis)

The raccoon (Procyon lotor) is the definitive host of Baylisascaris procyonis, a large intestinal roundworm that is zoonotic and can result in fatal or severe central nervous system disease in young children. Prevalence of infection among raccoon populations often is high, and in the midwestern United States, B. procyonis has been reported in 68-82% of raccoons. Raccoon populations have increased in response to changes in human land use, and often reach higher densities in urban and suburban landscapes than rural landscapes. However, shifts in foraging behavior among urban raccoons could impact the transmission of B. procyonis if small vertebrate intermediate hosts are not a significant part of the raccoon diet. The objective of this study was to compare prevalence of B. procyonis infection between urban and rural raccoon populations on a regional scale. Necropsy was done on 204 raccoons collected from September through February during 2000-2005 from seven states across the Midwest (regional sample). Baylisascaris procyonis was found in 54% of examined raccoons. Prevalence differed between land-use types (chi2=11.56, df=1, P=0.0007), and was higher among animals collected from rural locations (65%) than those collected in urban locations (41%). Intensity of infection also differed (F=5.52, df=1, P=0.02), with rural raccoons having greater worm burdens (x=29.63+/-36.42) than urban raccoons (x=13.85+/-18.47). Despite high densities of raccoons in urban landscapes, fewer urban raccoons were infected with B. procyonis, suggesting decreased dependence on intermediate hosts as a food source. This possible explanation was supported by a similar trend in prevalence among subsamples of raccoons collected from three Chicago-area populations (local samples) with differing levels of urbanization, population densities, and foraging behavior that had been intensively monitored during 1995-2002. Decreased transmission of B. procyonis in urban landscapes may be due to decreased predation of intermediate hosts, and contact of juvenile raccoons with B. procyonis eggs may be an important factor in maintaining infections within such populations.     

Eimeria and sarcocystis in raccoons in Illinois

Eimeria nuttalli oocysts were found in 58% (21/36) and E. procyonis oocysts in 25% (9/36) of raccoons Procyon lotor in Illinois, and sporocysts of Sarcocystis sp. in 17% (2/12) of other raccoons in Illinois. The oocysts of E. nuttalli were ellipsoidal to ovoid, 15-21 X 12-17 micrometer, with a one-layered, smooth, colorless wall. The oocysts of E. procyonis were 22-28 X 18-22 micrometer, with a rough, striated, brownish, two-layered wall. The sporulated sporocysts of Sarcocystis sp. were 11-13 X 8-10 micrometer. Attempts to infect baby pigs by feeding them sporocysts of Sarcocystis sp. from the reaction failed.     

Gnathostoma procyonis from south Georgia and north Florida raccoons

From 2004 to 2006, 511 raccoons collected by the United States Department of Agriculture Wildlife Services as part of a study to evaluate the effects of mesomammalian predator removal on bobwhite-quail reproduction, were examined for the presence of Gnathostoma procyonis, a nematode that parasitizes the stomach of its definitive host, the raccoon. One hundred forty-one raccoons (27.6%) contained G. procyonis, with males being equally infected (27.5%) as females (27.8%). Mean intensity did not differ significantly between sexes (males-mean = 2.88, range 1-17; females-mean = 2.78, range 1-10) or between collection sites. A significant seasonal prevalence of G. procyonis was noted with a peak in March (43.3%, n = 120) and a minimum in September (5.4%, n = 37). Both collection sites exhibited significant seasonal decreases in G. procyonis, but were not significantly different from each other. There was no cumulative seasonal pattern in mean intensity of G. procyonis, and no seasonal pattern at either collection site. Host weight was not related to either G. procyonis prevalence or mean intensity. Host removal did not have an apparent effect on prevalence or mean intensity of G. procyonis.     

Helminths of the raccoon (Procyon lotor) in western Kentucky

Seventy raccoons (Procyon lotor) from western Kentucky were examined for helminths from December 1985 through May 1986. Twenty-three species of helminths were collected including 10 species of Trematoda (Brachylaima virginiana, Euryhelmis squamula, Eurytrema procyonis, Fibricola cratera, Gyrosoma singulare, Maritreminoides nettae, Mesostephanus appendiculatoides, Metagonimoides oregonensis, Paragonimus kellicotti, Pharyngostomoides procyonis), 2 species of Cestoda (Atriotaenia procyonis, Mesocestoides variabilis), 10 species of Nematoda (Arthrocephalus lotoris, Baylisascaris procyonis, Capillaria putorii, C. plica, Crenosoma goblei, Dracunculus insignis, Gnathostoma procyonis, Molineus barbatus, Physaloptera rara, Trichinella spiralis), and 1 species of Acanthocephala (Macracanthorhynchus ingens). A mean of 6.4 (3-11) helminth species per host was recorded. Fibricola cratera, Atriotaenia procyonis, Mesocestoides variabilis, Arthrocephalus lotoris, Capillaria plica, Dracunculus insignis, Molineus barbatus, and Physaloptera rara were ubiquitous parasites of the raccoon, whereas specific nidi were observed for Eurytrema procyonis, Gyrosoma singulare, Paragonimus kellicotti, Baylisascaris procyonis, Trichinella spiralis, and Macracanthorhyncus ingens. With an overall prevalence of 10% or higher, 15 of the 23 helminth species were considered common parasites of the raccoon in western Kentucky. When the 10% prevalence rate was applied within geographical quadrants to correct for the presence of nidi it was found that 18 of the 23 helminth species were common and 5 were regarded as rare parasites of the raccoon. Two species of nematodes, T. spiralis and B. procyonis, displayed a markedly higher prevalence in male raccoons.     

Clinical coccidiosis in raccoons (Procyon lotor)

Clinical coccidiosis was diagnosed in wild-caught and captive raccoons. Eimeria procyonis-like oocysts were seen in 15 of 15 captive raccoons. In 6 of 6 juvenile wild-caught raccoons examined at necropsy, endogenous coccidian stages were seen in the small intestine. Two types of schizonts (large and small) were identified. Large schizonts were up to 110 microm long, contained 10-microm-long merozoites, and were in crypt glandular epithelial cells. Smaller schizonts were 10 microm long, contained 5-microm-long merozoites, and were at the tips of the villi. Only a few gamonts and no oocysts were seen in sections. These stages were thought to be of E. procyonis.     

Cryptosporidium sp. skunk genotype in wild raccoons (Procyon lotor) naturally infected with Baylisascaris procyonis from Central Germany

Cryptosporidium spp. are apicomplexan parasites of public health concern. They are one of the main causes of intestinal diseases in humans and animals. Contaminated water is among the main sources of infection for humans and mammals. Raccoons are an introduced species in Germany. They are anthropogenic adapters with a natural affinity for water bodies. We collected samples from wild raccoons in the Federal States of Saxony and Thuringia, Central Germany. Through molecular genotyping, we found Cryptosporidium sp. skunk genotype in one raccoon from Saxony (1/24) and in one animal from Thuringia (1/27). Both raccoons were also infected with the zoonotic nematode Baylisascaris procyonis. This is the first report of co-infection with these two parasites in raccoons from Germany. Our study highlights the potential of these animals as carriers of zoonotic pathogens. Since raccoons can thrive in human settlements, this study provides data that can be used as a baseline for preventive programs.     

Changes in transmission of Baylisascaris procyonis to intermediate hosts as a function of spatial scale

Physical changes in landscapes alter the abundance and distribution of species. Higher-order effects can occur when changes in ecological processes result in altered interspecific interactions and subsequent changes in a species' abundance or persistence. Baylisascaris procyonis , a roundworm parasite of raccoons ( Procyon lotor ), is pathogenic to numerous small vertebrates that serve as intermediate hosts, including white-footed mice ( Peromyscus leucopus ). Raccoons have responded positively to agriculturally induced changes in landscapes, with potential consequences for intermediate hosts of B . procyonis . We examined white-footed mice from a homogeneous, predominantly forested landscape in south-central Indiana and a heterogeneous, predominantly agricultural landscape in northwestern Indiana for presence of larval B . procyonis . We compared prevalence of infection, intensity of infection, and average number of larvae per mouse between the landscapes, and among forest patches within the highly fragmented agricultural landscape. Prevalence, intensity of infection, and average number of larvae were significantly higher in the highly fragmented landscape. Within the agricultural landscape, regression models predicted probability of infection, intensity of infection, and average number of larvae per mouse per patch as functions of forest patch area and isolation. We conclude that positive responses of raccoons to agriculturally induced fragmentation of forests have resulted in increased encounter rates between white-footed mice and infective stages of B . procyonis between and within landscapes, resulting in increased transmission of the parasite to intermediate hosts.     

Periodontal and dental lesions in raccoons from a farming and a recreational area in Illinois

Dental health was evaluated in two populations of raccoons (Procyon lotor) in western Illinois (USA); one was from a rural agricultural area with low human density and the other from a nearby state park heavily used by humans and raccoons. From 1989 through 1993, 300 raccoons were live-trapped in the agricultural area and 246 raccoons were live-trapped in the park. Oral health was assessed using gingival and calculi indices and by measuring loss of attachment and tooth wear. Raccoons from the park were significantly older and smaller, but not thinner, than raccoons from the farmed area. Gingival and periodontal indices, tooth wear, tooth loss, and caries increased significantly from juveniles to yearlings to adults, at both sites. Males had higher levels of gingivitis and loss of periodontal attachment than females, but were similar on other dental measures. There were no seasonal differences between raccoons in dental indices. Animals with high scores for one oral measure tended to have high values for all indices. Dental health was generally good for juveniles and yearlings from both sites. Among adults, periodontal indices and the prevalence of caries were significantly higher in the park, but prevalence of broken or missing teeth was similar for both populations. There was no association between body condition, and a higher dental score or more missing or broken teeth.     

Proposed field evaluation of a rabies recombinant vaccine for raccoons (Procyon lotor): site selection, target species characteristics, and placebo baiting trials

Prior to a limited field application of an orally-administered vaccinia-rabies glycoprotein (V-RG) recombinant virus vaccine for wildlife, background data were obtained for the proposed site on Parramore Island, Virginia (USA). Mammalian target and nontarget species, potentially at risk for exposure to vaccine were inventoried. Placebo baiting trials with a fishmeal polymer bait resulted in high bait disturbance (88 to 100%), primarily by raccoons (Procyon lotor), with infrequent visitation and no evidence of bait consumption by deer (Odocoileus virginianus), small mammals or avian species. Definitive bait acceptance rates by raccoons (indicative of bait ingestion) were difficult to accurately determine based exclusively on premolar and vibrissae samples collected antemortem from live-trapped raccoons for tetracycline and rhodamine B biomarker analyses, respectively. Bait acceptance rate was more accurately determined during a pilot baiting trial conducted on North Island, South Carolina, when mandibles (postmortem samples) were examined for tetracycline incorporation. Parasitologic findings in raccoons on Parramore Island included Hepatozoan procyonis, Phagicola angrense and Physaloptera rara and a variety of incidental microscopic lesions, and provided baseline pathological data for comparison subsequent to V-RG vaccine application. A population density estimate of one raccoon/2.7 ha was calculated using mark-recapture data for comparison after vaccine deployment. Limited reproductive data, including estimates of pregnancy rates by palpation, the number of live kits/litter live-trapped with previously pregnant raccoons or observed in the dens of radio-collared raccoons, was gathered to assess the effect of proposed oral vaccination with V-RG vaccine. Home ranges were assessed by radio-telemetry of 15 raccoons; all radio-collared raccoons currently reside on Parramore Island.(ABSTRACT TRUNCATED AT 250 WORDS)     

Fatal Baylisascaris larva migrans in a colony of Japanese macaques kept by a safari-style zoo in Japan

A colony of Japanese macaques (Macaca fuscata fuscata) kept by a safari-style zoo in Japan experienced 9 sporadic cases of fatal neurological diseases, such as epilepsy and posterior paralysis, during the 12 yr from 1989 to 2001. This macaque colony consisted of approximately 30 animals, on average, during this period, and the macaques shared their living space with II American black bears (Ursus americanus) harboring zoonotic roundworms (Baylisascaris transfuga). Close to this enclosure, a cote for 2-3 raccoons (Procyon lotor) was placed, and raw sewage from this cote ran into a shallow drain in the area for macaques and bears. However, fecal examinations in recent years did not detect the infection of raccoons with zoonotic roundworms (Baylisascaris procyonis). Postmortem histological examination of the latest 2 ill macaques detected multifocal malacia in the brain; 2 ascarid larvae of 60 microm maximum width were encapsulated in the cerebrum and lungs of 1 of the animals. To determine the causative ascarid species of the fatal larva migrans, we analyzed 2 additional encapsulated Baylisascaris larvae collected from formalin-fixed lungs by morphological and molecular approaches. This sporadic outbreak is the second record of Baylisascaris larva migrans in animals in Japan.     

Capillaria procyonis (Nematoda: Trichuroidea) eggs from the tongue of the raccoon (Procyon lotor)

During an investigation to determine the prevalence and intensity of larvae of Trichinella spiralis in raccoons (Procyon lotor), unembryonated capillariid-type eggs were found routinely in the sediment resulting from 1% pepsin-HCl acid digests of the tongue. The sediment from 36 (90%) of the 40 tongue digests examined contained these capillariid-type eggs. Mean measurements of egg width and length were 25 +/- 2 microns and 62 +/- 2 microns, respectively. In addition, the surface of the egg shell had a pitted appearance. Adult parasites were not found in any of the tongue digests. The egg measurements and surface topography agree with what has been described previously and are tentatively identified as Capillaria procyonis. The detection of C. procyonis eggs in the present report indicates that this parasite inhabits the epithelial lining of the raccoon tongue, in addition to the esophagus, and that eggs expelled by females are deposited in the tracts these parasites create as they migrate.     

Severe and fatal central nervous system disease in humans caused by Baylisascaris procyonis, the common roundworm of raccoons: a review of current literature

Baylisascaris procyonis, a parasitic infection of raccoons, causes severe neurologic disease in humans when infective eggs from raccoon feces are ingested. Definitive diagnosis is challenging, but can be made by isolation of larvae in brain biopsy or exclusion of other potential causes of eosinophilic meningoencephalitis. Prevention efforts are critical due to the lack of effective treatment.     

Prevalence of patent Baylisascaris procyonis infection in raccoons (Procyon lotor) in Ithaca, New York

The prevalence of patent Baylisascaris procyonis infection in raccoons was determined by examining fecal samples collected between July 1986 and May 1987 in Ithaca, New York. September, October, and November had the highest prevalence of infection (35-48%). Significant differences (P less than 0.001) were found when months were grouped by season to test the hypothesis that a fecal sample's probability of being positive does not vary from month to month. Fall was the season contributing most to the overall chi-square statistic. Host sex/age class and prevalence of patent infection were investigated. The raccoons were aged as either juveniles or adults. A significantly higher prevalence of patent infection (P less than 0.001) was found in juveniles when compared to adults. No statistically significant difference was found in other comparisons of host sex and age. Contingency analysis tested the independence of sex/age class/season and presence of eggs. The results of the test were significant (P less than 0.001).     

Lost and found: Helminths infecting invasive raccoons introduced to Italy

North American raccoons (Procyon lotor) have been introduced to several European countries, where they may represent a sanitary threat as hosts of several pathogens such as the zoonotic ascarid Baylisascaris procyonis. We carried out parasitological analysis on raccoons introduced to Italy to verify whether the species had carried along B. procyonis or any other gastro-intestinal helminths that may threaten humans, livestock or native wildlife. We examined 64 raccoons culled in Northern Italy during control activities and 3 roadkills opportunistically sampled from a separate population located in central Italy. Helminths were collected from the gastro-intestinal tract through standard parasitological techniques and identified based on a combination of morphology and molecular methods. Overall, examined raccoons showed a poor parasitic fauna, with almost 30% of individuals free of any helminth infection. The most prevalent species were the nematodes Strongyloides procyonis (26.9%), Aonchotheca putorii (25.4%) and Porrocaecum sp. (19.4%). Plagiorchis sp. trematodes were also common (13.4%), whereas cestodes were scarcely represented. With the exception of S. procyonis introduced from North America, all the other identified taxa have either a Eurasian or a wide Holarctic distribution. Despite not finding any B. procyonis in the examined raccoons, passive surveillance for this parasite should be implemented, especially in Tuscany, since the limited host sample examined in the present survey does not allow to exclude its presence.     

Implications of raccoon latrines in the epizootiology of baylisascariasis.

Raccoons (Procyon lotor) frequently establish defecation sites, termed latrines, on large logs, stumps, rocks, and other horizontally oriented structures/surfaces. These latrines are important foci of infective eggs of Baylisascaris procyonis, a nematode parasite of raccoons which is pathogenic to numerous species of mammals and birds. To examine the role of raccoon latrines in this animal-parasite interaction, we documented animal visitations to raccoon latrines in two large forested tracts and two woodlots in Indiana (USA) during 1994 and 1995. Species richness of vertebrate visitors did not differ between sites or years, but species composition differed by site and year. Fourteen mammal and 15 bird species were documented visiting raccoon latrines. Small granivorous mammals, including white-footed mice (Peromyscus leucopus), eastern chipmunks (Tamias striatus), and tree squirrels (Sciurus carolinensis, S. niger, Tamiasciurus hudsonicus) were the most common visitors to latrine sites. White-footed mice, chipmunks, white-breasted nuthatches (Sitta carolinensis), and opossums (Didelphis virginiana) were photographed foraging on undigested seeds in raccoon feces. Active foraging at latrines also was shown experimentally; seeds embedded in raccoon feces were removed at a greater rate at latrine sites than at nonlatrines. We conclude that raccoon latrines are visited routinely by a variety of vertebrates, especially small granivorous rodents and birds which forage for seeds in raccoon feces, and that raccoon latrines are probable sites of transmission of B. procyonis to susceptible mammals and birds.