Literature DB >> 27869612

Baylisascaris procyonis Roundworm Seroprevalence among Wildlife Rehabilitators, United States and Canada, 2012-2015.

Sarah G H Sapp, Lisa N Rascoe, Patricia P Wilkins, Sukwan Handali, Elizabeth B Gray, Mark Eberhard, Dana M Woodhall, Susan P Montgomery, Karen L Bailey, Emily W Lankau, Michael J Yabsley.   

Abstract

Baylisascaris procyonis roundworms can cause potentially fatal neural larva migrans in many species, including humans. However, the clinical spectrum of baylisascariasis is not completely understood. We tested 347 asymptomatic adult wildlife rehabilitators for B. procyonis antibodies; 24 were positive, suggesting that subclinical baylisascariasis is occurring among this population.

Entities:  

Keywords:  Ascaridoidea; Baylisascaris procyonis; Canada; United States; ascarid roundworm; baylisascariasis; larva migrans; occupational illnesses; parasites; raccoons; roundworms; seroprevalence; wildlife; wildlife rehabilitators; zoonoses

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Substances:

Year:  2016        PMID: 27869612      PMCID: PMC5189140          DOI: 10.3201/eid2212.160467

Source DB:  PubMed          Journal:  Emerg Infect Dis        ISSN: 1080-6040            Impact factor:   6.883


Baylisascaris procyonis, a roundworm of raccoons (Procyon lotor) and rarely dogs, can cause fatal neural larva migrans or ocular larval migrans in numerous bird and mammal species, including humans (). At least 54 human cases have been reported; however, cases may not have been recognized or reported, especially ocular cases, for which parasite identification is rare (–). Most diagnosed cases have been in children and were severe or fatal. Treatment is difficult after onset of neurologic symptoms, and neural larva migrans survivors may have permanent neurologic sequelae (). The clinical spectrum of baylisascariasis is not fully understood. Limited evidence suggests that subclinical disease may occur (,,,). Baylisascaris larvae were an incidental finding in the brain of an Alzheimer disease patient (), and B. procyonis antibodies were reported in the parents of a child with baylisascariasis and in 4 of 13 adults in Germany with raccoon contact; assay specificity was not reported (,). The occurrence of subclinical infections with related ascarids (e.g., Toxocara species) is well established; up to 14% of persons in the United States are seropositive, although it is unknown how many have clinical manifestations (). Wildlife rehabilitators may represent a population at risk for subclinical baylisascariasis due to frequent contact with raccoons and their feces, which may contain infectious larvated B. procyonis eggs. We assessed the occurrence of antibodies to B. procyonis in a sample of wildlife rehabilitators from the United States and Canada and administered a questionnaire on rehabilitation experience and procedures.

The Study

During 2012–2015, we collected serum samples from and administered questionnaires to wildlife rehabilitators (details in Technical Appendix). We tested serum samples for B. procyonis IgG using a recombinant B. procyonis repeat antigen 1 protein Western blot as described (). Of 347 enrolled persons (Table 1), 315 (91%) reported current involvement in rehabilitation activities. Participants had an average of 10.5 (median 7.0) years of animal rehabilitation experience. Most respondents (92%) reported having contact with raccoons at some point; 64% reported actively rehabilitating raccoons in the past year (Table 2).
Table 1

Demographic characteristics of participants in a study of Baylisascaris procyonis roundworm seroprevalence among wildlife rehabilitators, United States and Canada, 2012–2015

VariableNo. (%) respondents, N = 347No. (%) seropositive
Sex
Female299 (86.2)21 (7.0)
Male
48 (13.8)
3 (6.3)
Race
Asian6 (1.7)0
American Indian or Alaska Native1 (0.3)0
Black or African American1 (0.3)0
White327 (94.2)23 (7.0)
Other2 (0.6)0
Multiracial
10 (2.9)
1 (10.0)
Ethnicity
Hispanic5 (1.4)0
Not Hispanic315 (90.8)19 (6.0)
Declined to state
27 (7.8)
5 (18.5)
Geographic region of rehabilitation activities*
Northeastern106 (30.5)4 (3.8)
Midwestern74 (21.3)8 (10.8)
Central23 (6.6)0
Southern110 (31.7)5 (4.5)
Western34 (9.8)7 (20.6)

*Geographic regions are defined as follows: Northeastern: Delaware, Maryland, Massachusetts, Maine, New Jersey, New York, Pennsylvania, and Virginia, USA, and Quebec Province, Canada; Midwestern: Illinois, Indiana, Kentucky, Michigan, Minnesota, Missouri, Ohio, and Wisconsin , USA, and Manitoba and Ontario Provinces, Canada; Central: Arizona, Colorado, Kansas, Oklahoma, and Texas, and Alberta, Province, Canada; Southern: Alabama, Florida, Georgia, Louisiana, Mississippi, North Carolina, South Carolina, and Tennessee, USA; and Western: California, Oregon, and Washington, USA, and British Columbia Province, Canada.

Table 2

Rehabilitation work characteristics and experience of wildlife rehabilitators enrolled in a study of Baylisascaris procyonis roundworm seroprevalence among wildlife rehabilitators, United States and Canada, 2012–2015

VariableNo. (%) respondentsNo. (%) seropositive
Involvement in wildlife rehabilitation, N = 347
Currently involved314 (90.5)22 (7.0)
Formerly involved19 (5.5)0 (0)
Other raccoon contact
14 (4.0)
2 (14.3)
Rehabilitation experience, y, N = 322
<2.048 (14.9)2 (4.2)
2.0–4.996 (29.8)7 (7.3)
5.0–9.967 (20.8)1 (1.5)
10.0–20.064 (19.9)8 (12.5)
>20.0
47 (14.6)
3 (6.4)
Raccoon rehabilitation, N = 347
Rehabilitated raccoons in past year222 (64.0)16 (7.2)
Rehabilitated raccoons (prior to past year)41 (11.8)2 (4.9)
Never rehabilitated raccoons
84 (24.2)
6 (7.1)
General raccoon contact, N = 329
Had contact in past year266 (80.9)19 (7.1)
Had contact ever36 (10.9)3 (8.3)
Never had contact
27 (8.2)
2 (7.4)
B. procyonis prevalence among raccoons in state or province of residence, N = 347*
Very high (>50%)79 (22.8)14 (21.5)
High (25%–49%)127 (36.6)5 (4.6)
Medium (10%–24%)92 (26.5)4 (4.3)
Low (<10%), sporadic, or unknown49 (14.1)1 (2.1)

*Prevalence levels in the various US states and Canadian Provinces are shown in the Figure.

*Geographic regions are defined as follows: Northeastern: Delaware, Maryland, Massachusetts, Maine, New Jersey, New York, Pennsylvania, and Virginia, USA, and Quebec Province, Canada; Midwestern: Illinois, Indiana, Kentucky, Michigan, Minnesota, Missouri, Ohio, and Wisconsin , USA, and Manitoba and Ontario Provinces, Canada; Central: Arizona, Colorado, Kansas, Oklahoma, and Texas, and Alberta, Province, Canada; Southern: Alabama, Florida, Georgia, Louisiana, Mississippi, North Carolina, South Carolina, and Tennessee, USA; and Western: California, Oregon, and Washington, USA, and British Columbia Province, Canada. *Prevalence levels in the various US states and Canadian Provinces are shown in the Figure.
Figure

Locations for participant sampling in a study of Baylisascaris procyonis roundworm seroprevalence among wildlife rehabilitators, United States and Canada, 2012–2015. Yellow dots indicate counties (USA) or township/municipality (Canada) in which enrolled persons reported practicing wildlife rehabilitation. Red dots indicate locations of seropositive persons. Shading of states/provinces indicates general state/province level prevalence of B. procyonis in raccoons based on published reports (,–).

Twenty-four (7%; 95% CI 4.7%–10.1%) participants tested positive for B. procyonis antibodies; adjusted prevalence, considering assay performance characteristics, was 5.7% (95% CI 2.2%–9.2%) (Figure) (). Of those 24 participants, 22 (92%) were actively rehabilitating wildlife; the other 2 reported occasional wildlife contact, including contact with raccoons, through veterinary clinic activities. All but 2 seropositive persons reported raccoon contact, and 2 practiced rehabilitation in the same household. Nineteen (79%) of the 24 seropositive persons resided in a US state or Canadian province classified as having very high or high B. procyonis prevalence among raccoons (Table 2). Locations for participant sampling in a study of Baylisascaris procyonis roundworm seroprevalence among wildlife rehabilitators, United States and Canada, 2012–2015. Yellow dots indicate counties (USA) or township/municipality (Canada) in which enrolled persons reported practicing wildlife rehabilitation. Red dots indicate locations of seropositive persons. Shading of states/provinces indicates general state/province level prevalence of B. procyonis in raccoons based on published reports (,–).

Conclusions

We detected antibodies to B. procyonis roundworms in 7% of wildlife rehabilitators we tested, suggesting that exposure to this zoonotic parasite may occur without clinical disease. Participants reported various degrees of raccoon contact. Although the transmission source could not be determined (i.e., from rehabilitation of raccoons or from exposure to eggs during other activities), use of gloves and handwashing was generally inconsistent among the seropositive persons in this study (S.G.H. Sapp, data not shown). B. procyonis is transmitted by ingestion of larvated eggs; thus, proper use of personal protective equipment (PPE), adherence to cleaning and disinfection protocols, and proper hand hygiene should minimize the risk associated with exposure to feces. Transmission risk can also occur when handling animals whose fur has been contaminated by infective raccoon eggs, as shown for Toxocara canis parasites and dog fur (). More investigations are needed regarding the occurrence of B. procyonis eggs on raccoon fur and transmission implications. Lapses in PPE use and hand hygiene may indicate a lack of caution or risk awareness for other pathogens. Wildlife rehabilitators in areas with a very high prevalence of B. procyonis infection among raccoons may be at elevated risk for subclinical infections. Only 1 B. procyonis–seropositive wildlife rehabilitator resided in a state with low or sporadic prevalence (Alabama); however, that person lived in an area adjacent to a Florida county where the prevalence of B. procyonis infection in raccoons was 9% (M.J. Yabsley, unpub. data) (Figure). Data on B. procyonis prevalence in raccoons are outdated or missing for many US states and Canadian provinces. Furthermore, raccoon infections with B. procyonis are now being reported in areas where the parasite has historically been absent (e.g., the southeastern United States); thus, awareness of this parasite may be limited in those areas (). More surveillance is needed on the distribution and prevalence of B. procyonis infection among raccoons to assess the association with exposure risks among humans. Rehabilitation facilities housing raccoons can easily be contaminated with B. procyonis because high numbers of environmentally hardy eggs are passed by infected raccoons (). Our finding of 2 seropositive raccoon rehabilitators operating out of the same household highlights the importance of infection-control practices. Facility contamination can be prevented by treating raccoons for parasites at intake and at regular intervals thereafter and by sterilizing enclosures using heat-based methods (). Several anthelmintic drugs can kill adult B. procyonis, but raccoons with high worm burdens may require retreatment (). Raccoon enclosures and housing should be constructed with materials that are easy to clean and disinfect using heat-based methods. We tested persons with wildlife (mostly raccoon) contact, so our results describe an exposure risk that likely does not apply to the general public. However, persons in other occupations or activities (e.g., zoo keepers, wildlife biologists) may have similar exposure risks. Domestic dogs, other wildlife species (e.g., skunks, bears), and some exotic pets (e.g., kinkajous) are hosts for Baylisascaris spp. parasites and may present exposure risks (). Although the assay we used has a sensitivity of 88% and specificity of 98%, it is time-consuming and not ideal for large-scale epidemiologic studies (). Development of a high-quality ELISA would facilitate larger epidemiologic studies on the risk for baylisascariasis among different demographic groups and help further elucidate specific risk factors. Our study had several limitations. We used a convenience sampling, so not all regions were well represented, and sample size was relatively small. Our prevalence estimate may be inflated because positive predictive value is reduced in populations in which prevalence is low. The assay we used is the reference standard for clinical diagnosis but has not been used to test asymptomatic persons. Although an association between human B. procyonis exposure and seroconversion has not been established, asymptomatic seropositive infections would be expected because clinical disease probably occurs only when larvae cause damage to neural tissue or eyes (). An estimated 95% of migrating larvae enter muscle or visceral organs, where they may stimulate an immune response but not cause clinical disease (). In support of this presumption, the assay we used indicated that experimental infections of Peromyscus rodents with low numbers of B. procyonis parasites resulted in no clinical disease with seroconversion (S.G.H. Sapp, unpub. data). Last, participants were primarily licensed rehabilitators who belonged to professional organizations, and many practiced rehabilitation in large, dedicated facilities. Such facilities generally have safety protocols that may encourage more consistent PPE use and awareness of zoonotic diseases, so the risk for infection may be greater in smaller or informal rehabilitation settings. To prevent infection with B. procyonis parasites, proper PPE and hand hygiene practices should be used consistently when handling animals and when contact with animal feces might occur. Education materials and outreach efforts discussing PPE use, infection control, and zoonotic pathogens should be directed to wildlife rehabilitators to increase awareness of potential occupational risks.

Technical Appendix

Details regarding participant enrollment, acquisition of samples, serologic testing, and data analysis in a study of Baylisascaris procyonis roundworm seroprevalence among wildlife rehabilitators, United States and Canada, 2012–2015.
  13 in total

1.  Exact confidence limits for prevalence of a disease with an imperfect diagnostic test.

Authors:  J Reiczigel; J Földi; L Ozsvári
Journal:  Epidemiol Infect       Date:  2010-03-03       Impact factor: 2.451

Review 2.  Ocular parasitic diseases: a review on toxocariasis and diffuse unilateral subacute neuroretinitis.

Authors:  Rafael T Cortez; Gema Ramirez; Lucienne Collet; Gian Paolo Giuliari
Journal:  J Pediatr Ophthalmol Strabismus       Date:  2010-07-22       Impact factor: 1.402

3.  Interlaboratory optimization and evaluation of a serological assay for diagnosis of human baylisascariasis.

Authors:  Lisa N Rascoe; Cynthia Santamaria; Sukwan Handali; Sriveny Dangoudoubiyam; Kevin R Kazacos; Patricia P Wilkins; Momar Ndao
Journal:  Clin Vaccine Immunol       Date:  2013-09-18

4.  Efficacy of six anthelmintics against luminal stages of Baylisascaris procyonis in naturally infected raccoons (Procyon lotor).

Authors:  C Bauer; A Gey
Journal:  Vet Parasitol       Date:  1995-11       Impact factor: 2.738

5.  Diagnosis and management of Baylisascaris procyonis infection in an infant with nonfatal meningoencephalitis.

Authors:  C K Cunningham; K R Kazacos; J A McMillan; J A Lucas; J B McAuley; E J Wozniak; L B Weiner
Journal:  Clin Infect Dis       Date:  1994-06       Impact factor: 9.079

6.  National seroprevalence and risk factors for Zoonotic Toxocara spp. infection.

Authors:  Kimberly Y Won; Deanna Kruszon-Moran; Peter M Schantz; Jeffrey L Jones
Journal:  Am J Trop Med Hyg       Date:  2008-10       Impact factor: 2.345

7.  Surveillance for Baylisascaris procyonis in raccoons (Procyon lotor) from Wyoming, USA.

Authors:  Michael J Pipas; L Kristen Page; Kevin R Kazacos
Journal:  J Wildl Dis       Date:  2014-07-11       Impact factor: 1.535

8.  Baylisascaris procyonis infection in elderly person, British Columbia, Canada.

Authors:  Tawny Hung; Ronald C Neafie; Ian R A Mackenzie
Journal:  Emerg Infect Dis       Date:  2012-02       Impact factor: 6.883

9.  Viability of Baylisascaris procyonis Eggs.

Authors:  Shira C Shafir; Frank J Sorvillo; Teresa Sorvillo; Mark L Eberhard
Journal:  Emerg Infect Dis       Date:  2011-07       Impact factor: 6.883

10.  Geographic expansion of Baylisascaris procyonis roundworms, Florida, USA.

Authors:  Emily L Blizzard; Michael J Yabsley; Margaret F Beck; Stefan Harsch
Journal:  Emerg Infect Dis       Date:  2010-11       Impact factor: 6.883

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1.  First detection of Baylisascaris procyonis in wild raccoons (Procyon lotor) from Leipzig, Saxony, Eastern Germany.

Authors:  Zaida Rentería-Solís; Stefan Birka; Ronald Schmäschke; Nina Król; Anna Obiegala
Journal:  Parasitol Res       Date:  2018-06-27       Impact factor: 2.289

2.  Detection and Evaluation of Antibody Response to a Baylisascaris-Specific Antigen in Rodent Hosts with the Use of Western Blotting and Elisa.

Authors:  Sarah G H Sapp; Sukwan Handali; Sara B Weinstein; Michael J Yabsley
Journal:  J Parasitol       Date:  2018-08-29       Impact factor: 1.276

Review 3.  Beyond the raccoon roundworm: The natural history of non-raccoon Baylisascaris species in the New World.

Authors:  Sarah G H Sapp; Pooja Gupta; Melissa K Martin; Maureen H Murray; Kevin D Niedringhaus; Madeleine A Pfaff; Michael J Yabsley
Journal:  Int J Parasitol Parasites Wildl       Date:  2017-04-30       Impact factor: 2.674

4.  Helminthes in Feral Raccoon (Procyon lotor) as an Alien Species in Iran.

Authors:  Meysam Sharifdini; Omar M Amin; Keyhan Ashrafi; Nader Karamzadeh; Iraj Mobedi; Behnaz Rahmati; Zahra Hesari
Journal:  Iran J Parasitol       Date:  2020 Apr-Jun       Impact factor: 1.012

5.  Seroprevalence of Baylisascaris procyonis Infection among Humans, Santa Barbara County, California, USA, 2014-2016.

Authors:  Sara B Weinstein; Camille M Lake; Holly M Chastain; David Fisk; Sukwan Handali; Philip L Kahn; Susan P Montgomery; Patricia P Wilkins; Armand M Kuris; Kevin D Lafferty
Journal:  Emerg Infect Dis       Date:  2017-08       Impact factor: 6.883

6.  Controlling infection in predator-prey systems with transmission dynamics.

Authors:  M-G Cojocaru; T Migot; A Jaber
Journal:  Infect Dis Model       Date:  2019-12-12
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