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Baylisascaris procyonis: an emerging helminthic zoonosis. (Synopsis).



Baylisascaris procyonis, a roundworm roundworm, another name for a nematode. See phylum Nematoda.  infection of raccoons, is emerging as an important helminthic hel·min·thic
adj.
1. Of or relating to worms, especially parasitic worms.

2. Tending to expel worms.

n.
See anthelmintic.
 zoonosis Zoonosis Definition

Zoonosis, also called zoonotic disease refers to diseases that can be passed from animals, whether wild or domesticated, to humans.
, principally affecting young children. Raccoons have increasingly become peridomestic animals living in close proximity to human residences. When B. procyonis eggs are ingested by a host other than a raccoon raccoon, nocturnal New World mammal of the genus Procyon. The common raccoon of North America, Procyon lotor, also called coon, is found from S Canada to South America, except in parts of the Rocky Mts. and in deserts. , migration of larvae through tissue, termed larval migrans, ensues. This larval infection can invade the brain and eye, causing severe disease and death. The prevalence of B. procyonis infection in raccoons is often high, and infected animals can shed enormous numbers of eggs in their feces. These eggs can survive in the environment for extended periods of time, and the infectious dose of B. procyonis is relatively low. Therefore, the risk for human exposure and infection may be greater than is currently recognized.

**********

Baylisascaris procyonis, a ubiquitous roundworm infection of raccoons (Procyon lotor), is increasingly being recognized as a cause of severe human disease (1,2). B. procyonis has a widespread geographic distribution, with infection rates as high as 70% in adult raccoons and exceeding 90% in juvenile raccoons (3). As with other ascarids, eggs are excreted in feces and must develop externally, typically in soil, to become infectious. When raccoons ingest infective eggs, larvae will hatch, enter the wall of the small intestine, and subsequently develop to adult worms in the small bowel. However, ingestion of eggs by other host animals, especially rodents and other small mammals, results in extraintestinal migration of larvae (4); an estimated 5%-7% of larvae invade the brain (5). The migration of helminth helminth /hel·minth/ (hel´minth) a parasitic worm.

hel·minth
n.
A worm, especially a parasitic roundworm or tapeworm.


Helminth
A type of parasitic worm.
 larvae through tissue in suboptimal hosts is termed larva migrans and may affect the viscera viscera /vis·ce·ra/ (vis´er-ah) plural of viscus.

vis·cer·a
pl.n.
1. The soft internal organs of the body, especially those contained within the abdominal and thoracic cavities.
 (visceral larva migrans visceral larva migrans
n.
A disease, chiefly of children, caused by ingestion of nematode ova, usually of Toxocara canis, characterized by high eosinophilia and often liver enlargement, fever, cough, and hyperglobulinemia.
 [VLM 1. (architecture) VLM - Very Large Memory.
2. (networking) VLM - Virtual Loadable Module.
]), the eye (ocular larva migrans ocular larva migrans
n.
Visceral larva migrans involving the eyes, primarily of older children, and marked by decreased visual acuity and strabismus.
 [OLM olm: see mud puppy. ]), or the nervous system (neural larva migrans [NLM Software that runs in a NetWare server. Although NetWare servers store DOS and Windows applications, they do not execute them. All programs that run in a NetWare server must be compiled into the NLM format. They are typically written in C and use Novell's libraries. ] (6). Raccoons :may also become infected when they eat larvae that have become encapsulated in the tissues of rodents and other animals (3).

More than 90 species of wild and domesticated animals have been identified as infected with B. procyonis larvae (3). Outbreaks of fatal central nervous system disease caused by B. procyonis have occurred on farms and in zoos and research animal colonies and have affected commercial chickens, bob-white quail, guinea pigs, commercial pheasants, and domestic rabbits (7-11). Natural infections have also been recognized in dogs, rodents, porcupines, chinchillas, prairie dogs, primates, woodchucks, emus, foxes, and weasels (12-16). Experimental infection of a variety of nonhuman primates has also been reported (17).

Human Infection

B. procyonis infection of humans typically results in fatal disease or severe sequelae sequelae Clinical medicine The consequences of a particular condition or therapeutic intervention  (1,2,18-24; pers. comm., W. Murray). Clinical manifestations include eosinophilic eosinophilic /eo·sin·o·phil·ic/ (-fil´ik)
1. readily stainable with eosin.

2. pertaining to eosinophils.

3. pertaining to or characterized by eosinophilia.
 encephalitis, ocular disease, and esoinophilic cardiac pseudotumor. Elevated peripheral cerebrospinal fluid eosinophilia eosinophilia /eo·sin·o·phil·ia/ (e?o-sin?o-fil´e-ah) abnormally increased eosinophils in the blood.

e·o·sin·o·phil·i·a
n.
An increase in the number of eosinophils in the blood.
 can be detected in cases of meningoencephalitis meningoencephalitis /me·nin·go·en·ceph·a·li·tis/ (me-ning?go-en-sef?ah-li´tis) inflammation of the brain and meninges.

toxoplasmic meningoencephalitis
. Eleven recognized human cases, four of them fatal, have been reported (Table). The first human case was reported in 1984 in a 10-month-old infant with fatal eosinophilic meningoencephalitis (18). At autopsy, numerous granulomas containing larvae of B. procyonis were observed in several organs and tissues (18). The brain was the most heavily affected, with granulomas concentrated in the periventricular white matter, around the dentate dentate /den·tate/ (den´tat) notched; tooth-shaped.

den·tate
adj.
Edged with toothlike projections; toothed.
 nuclei, and along the cerebral and cerebellar cerebellar /cer·e·bel·lar/ (ser?e-bel´ar) pertaining to the cerebellum.
Cerebellar
Involving the part of the brain (cerebellum), which controls walking, balance, and coordination.
 cortices cor·ti·ces  
n.
A plural of cortex.
. Numerous granulomas and larvae were also found in the mesentery mesentery: see peritoneum.  and cardiac tissue. The infant's family lived in a rural, wooded area of Pennsylvania, and raccoons were nesting in unused chimneys at the time infection was acquired.

Four additional cases of eosinophilic encephalitis with similar pathologic characteristics have been documented. Magnetic resonance images from a human case of Baylisascaris encephalitis are shown in Figure 1. In patients who have survived central nervous system (CNS See Continuous net settlement.

CNS

See continuous net settlement (CNS).
) invasion, severe neurologic sequelae have resulted. In a fatal case, an eosinophilic cardiac pseudotumor, affecting principally the left ventricle, was observed at autopsy; no larvae or granulomas were found in any other tissue examined.

[FIGURE 1 OMITTED]

No effective therapy exists for the visceral form of B. procyonis larval infection. In an experimental model, mice treated with albendazole and diethylcarbamezine within 10 days after infection were protected from CNS disease (25); however, several anthelminthic Anthelminthic (also spelled anthelmintic)
A type of drug or herbal preparation given to destroy parasitic worms or expel them from the body.

Mentioned in: Dysentery, Trichinosis


anthelminthic

anthelmintic.
 agents have been used to treat human cases without success. Laser photocoagulation photocoagulation /pho·to·co·ag·u·la·tion/ (-ko-ag?u-la´shun) condensation of protein material by the controlled use of an intense beam of light (e.g.  has been successful in treating ocular infection (26).

Because the disease is transmitted by the fecal-oral route, human cases of B. procyonis infection typically occur in younger age groups, mainly infants, who often engage in oral exploration of their environment and are therefore more likely to be exposed to B. procyonis eggs. Raccoon activity near the patient's residence is often described. All but one of the reported patients to date have been male, however; there is no reason to believe that females are less susceptible to infection.

Diagnosis and Underrecognition of Infection

Diagnosis of B. procyonis infection is typically done through morphologic identification of larvae in tissue sections (27). However, accurate diagnosis requires experience in recognizing larval morphologic characteristics and differentiating among a number of possible larval nematode nematode
 or roundworm

Any of more than 15,000 named and many more unnamed species of worms in the class Nematoda (phylum Aschelminthes). Nematodes include plant and animal parasites and free-living forms found in soil, freshwater, saltwater, and even vinegar
 agents, including Toxocara canis, T. cati, Ascaris lumbricoides, and species of Gnathastoma, Angiostrongylus, and Ancylostoma, as well as larval cestode cestode: see Platyhelminthes; tapeworm.  infections such as cysticercosis cysticercosis /cys·ti·cer·co·sis/ (sis?ti-ser-ko´sis) infection with cysticerci. In humans, infection with the larval forms of Taenia solium.

cys·ti·cer·co·sis
n.
 and echinococcosis Echinococcosis Definition

Echinococcosis (Hydatid disease) refers to human infection by the immature (larval) form of tapeworm, Echinococcus. One of three forms of the Echinococcus spp., E.
 (6,27). Characteristic features of B. procyonis larvae in tissue include its relatively large size (60 [mu]) and prominent single lateral alae (27) (Figure 2). While serologic testing has been performed in some cases as supportive diagnostic evidence, no commercial serologic test is currently available (28,29). However, a presumptive diagnosis can be made on the basis of clinical (meningoencephalitis, diffuse unilateral subacute neuroretinitis [DUSN DUSN Diffuse Unilateral Subacute Neuroretinitis ], pseudotumor), epidemiologic (raccoon exposure), radiologic (white matter disease), and laboratory results (blood and CNS eosinophilia).

[FIGURE OMITTED]

Human baylisascariasis is probably underrecognized, and the full spectrum of clinical illness is unclear. The agent is unknown to most clinicians and typically is not considered in a differential diagnosis. In addition, confirming the diagnosis requires an effective biopsy specimen that must contain an adequate cross-section of a larva. Since small numbers of larvae can cause severe disease and larvae occur sporadically in tissue, a biopsy may frequently fail to include larvae; such a specimen will result in a negative finding. Moreover, larval morphologic characteristics may not be recognized or may be misidentified. The accurate diagnosis of parasites in tissues can be difficult even for trained microscopists, and mistaken identification, particularly of helminth larvae, is not uncommon (27). Finally, no commercial serologic test exists for the diagnosis of B. procyonis infection, and the sensitivity, specificity, and predictive value of available serologic tests are unknown. Evidence for underrecognition of larval B. procyonis infection can be found in several reported cases of DUSN caused by larvae compatible with B. procyonis and a case of eosinophilic meningoencephalitis reported in an infant in 1975 (26,30,31).

Infection Potential and Human Risk

Although relatively few human cases of baylisascariasis have been reported, several factors suggest that the likelihood of exposure and infection may be greater than is currently recognized. Raccoons have a widespread geographic distribution, and infection with B. procyonis is common in raccoon populations, with typically high prevalence rates observed. An infected raccoon can harbor numerous adult worms and may excrete excrete /ex·crete/ (eks-kret´) to throw off or eliminate by a normal discharge, such as waste matter.

ex·crete
v.
To eliminate waste material from the body.
 large numbers of eggs. A single adult female worm may produce an estimated 115,000 to 877,000 eggs per day, and an infected raccoon can shed as many as 45,000,000 eggs daily (3,4,32). In light of the relatively low infectious dose of B. procyonis (estimated to be [less than or equal to] 55,000 eggs) and the viability of the eggs in the environment for months to years, the infection potential is not insubstantial. Raccoons have increasingly become peridomestic animals living in close proximity to human residences and are among the fastest growing wildlife populations nationwide. These animals benefit from feeding on abundant pet food left accessible, either accidentally or intentionally, and their populations can thrive under such conditions. In one suburban area near the residence of a recent patient in northern California, the raccoon population was measured at 30 animals per quarter acre. Areas frequented by raccoons and used for defecation defecation
 or bowel movement

Elimination of feces from the digestive tract. Peristalsis moves feces through the colon to the rectum, where they stimulate the urge to defecate.
 were found in close proximity to human dwellings, and B. procyonis eggs are routinely recovered from these areas (1). Children, particularly toddlers, may be at particular risk of exposure.

Although baylisascariasis may indeed be underdiagnosed, asymptomatic human infection may be the typical response, and the limited number of cases reported may indicate that an unrecognized immune defect is necessary for severe infection to occur. The prevalence of asymptomatic infection in human populations has yet to be determined.

A Possible Agent of Bioterrorism

In an era of increasing concern about bioterrorism (33), certain characteristics of B. procyonis make it a feasible bioterrorist agent. The organism is ubiquitous in raccoon populations and therefore easy to acquire. Enormous numbers of eggs can be readily obtained, and these eggs can survive in an infectious form for prolonged periods of time. As with other ascarids, the eggs can remain viable in a dilute (0.5%-2%) formalin solution for all indefinite period of time, and animal studies suggest that B. procyonis has a relatively small infectious dose. Moreover, the organism causes a severe, frequently fatal infection in humans, and no effective therapy or vaccine exists. Introduction of sufficient quantities or B. procyonis eggs into a water system or selected food products could potentially result in outbreaks of the infection. A similar agent, Ascaris Ascaris /As·ca·ris/ (-ris) a genus of nematode parasites of the large intestine. A. lumbricoi´des causes ascariasis.
ascaris /as·ca·ris/ (-ris 
 suum, a roundworm of pigs, was used to intentionally infect four university students who required hospitalization after eating a meal that had been deliberately contaminated with a massive dose of eggs (34). Contamination of community water sources would be difficult since the eggs of B. procyonis are relatively large (80 [micro]m long by 65 [micro]m wide) and would be readily removed by standard filtration methods or the flocculation flocculation /floc·cu·la·tion/ (flok?u-la´shun) a colloid phenomenon in which the disperse phase separates in discrete, usually visible, particles rather than congealing into a continuous mass, as in coagulation.  and sedimentation techniques used by municipal water systems in the United States. However, posttreatment contamination or targeting of smaller systems could be possible.

Conclusion

Baylisascariasis is an emerging helminthic zoonosis with the potential for severe infection that may be a more important public health problem than is currently recognized. Educating the medical community is of paramount importance in helping to define the extent of infection. Physicians should consider B. procyonis infection in the differential diagnosis of patients with eosinophilic meningoencephalitis, DUSN, and eosinophilic pseudotumor. While infants and children have a higher probability of infection, all age groups are at risk. The public should be made aware of the potential risks of exposure to raccoons and raccoon feces. Raccoons should be discouraged as pets or should be routinely evaluated for B. procyonis infection and treated. However, screening and treatment may not be sufficient to prevent exposure, since the likelihood of reinfection reinfection /re·in·fec·tion/ (-in-fek´shun) a second infection by the same agent or a second infection of an organ with a different agent.

re·in·fec·tion
n.
 is high. The public should be discouraged from feeding raccoons and should ensure that possible food sources (such as pet food, water, and garbage) are protected from raccoon access. Further study of the impact of larval B. procyonis infection on human health is warranted. Development of a standardized serologic test for B. procyonis would allow epidemiologic studies of its prevalence and incidence and help determine factors associated with infection. A sensitive and specific test would also provide a noninvasive method of diagnosis. Finally, a better understanding of the pathogenesis of B. procyonis infection and efforts to develop effective treatment approaches are warranted.
Table. Reported human cases of larval Baylisascaris procyonis infection

Year (a)     Location       Age     Sex              Clinical

1980       Pennsylvania    10 mo    Male           Eosinophilic
                                                meningoencephalitis
1984         Illinois      18 mo    Male           Eosinophilic
                                                meningoencephalitis
1990         New York      13 mo    Male           Eosinophilic
                                                meningoencephalitis
1992        California     29 yr    Male    Diffuse unilateral subacute
                                                  neuroretinitis
1991          Germany      48 yr   Female   Diffuse unilateral subacute
                                                  neuroretinitis
1995       Massachusetts   10 yr    Male       Esoinophilic cardiac
                                                    pseudotumor
1996         Michigan      6 yr     Male    Chorioretinitis, neurologic
                                                     deficits
1996         Michigan      2 yr     Male           Eosinophilic
                                               meningoencephalitis,
                                                  chorioretinitis
1997        California     13 mo    Male           Eosinophilic
                                                meningoencephalitis
1998        California     11 mo    Male     Eosinophilic encephalitis
1999        California     17 yr    Male           Eosinophilic
                                                meningoencephalitis

Year (a)     Location           Outcome        Reference

1980       Pennsylvania          Fatal            17
1984         Illinois            Fatal            18
1990         New York      Severe neurologic      19
                               sequelae
1992        California      Ocular sequelae       21
1991          Germany       Ocular sequelae       22
1995       Massachusetts         Fatal            20
1996         Michigan      Severe neurologic      23
                               sequelae
1996         Michigan      Severe neurologic      23
                               sequelae
1997        California     Severe neurologic       2
                               sequelae
1998        California     Severe neurologic       1
                               sequelae
1999        California           Fatal            (b)

(a) year of onset or report.

(b) Pers. comm., W. Murray.


Acknowledgment

The authors thank Howard A. Rowley for graciously providing the images in Figure 1.

Dr. Sorvillo is Associate Professor, Department of Epidemiology, UCLA School of Public Health The UCLA School of Public Health is the graduate school of public health affiliated with UCLA, and is located within the Center for Health Sciences building on the UCLA campus. UCLA is located in the Westwood neighborhood of Los Angeles, California. . His research interests include the epidemiology and control of infectious diseases, particularly parasitic agents.

References

(1.) Park SY, Glaser C, Murray WJ, Kazacos KR, Rowley HA, Fredrick DR, et al. Raccoon roundworm (Baylisascaris procyonis) encephalitis: case report and field investigation. Pediatrics 2000;106:E56.

(2.) Rowley HA, Uht RM, Kazacos KR, Sakanari J, Wheaton WV, Barkovich AJ, et al. Radiologic-pathologic findings in raccoon roundworm (Baylisascaris procyonis) encephalitis. Am J Neuroradiol 2000;21:415-20.

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(4.) Hamann KJ, Kephart GM, Kazacos KR, Gleich GJ. Immunofluorescent localization of eosinophil eosinophil /eo·sin·o·phil/ (e?o-sin´o-fil) a granular leukocyte having a nucleus with two lobes connected by a thread of chromatin, and cytoplasm containing coarse, round granules of uniform size.  granule granule, in astronomy: see photosphere.  major basic protein in fatal human cases of Baylisascaris procyonis infection. Am J Trop Med Hyg 1989;40:291-7.

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adj.
1. Of, relating to, or caused by vermin.

2. Infested with vermin.



verminous

pertaining to, due to, or abounding in worms or in vermin.
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(12.) Kazacos KR, Appel GO, Thacker HL. Cerebrospinal nematodiasis in a woodchuck woodchuck or groundhog, common name of a North American species of marmot, Marmota monax. This large rodent is found in open woods and ravines throughout most of Canada and the NE United States.  suspected of having rabies. J Am Vet Med Assoc 1981;179:1102-4.

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(16.) Fitzgerald SD, White MR, Kazacos KR. Encephalitis in two porcupines due to Baylisascaris larval migration. J Vet Diagn Invest 1991;3:359-62.

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as·ca·rid
n.
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(23.) Kuchle M, Knorr HL, Medenblik-Frysch S, Weber A, Bauer C, Naumann GO. Diffuse unilateral subacute neuroretinitis syndrome in a German most likely caused by the raccoon roundworm, Baylisascaris procyonis. Graefes Arch Clin Exp Ophthalmol 1993;231:48-51.

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pe·di·at·ric
adj.
Of or relating to pediatrics.
 cases from Chicago, Illinois. American Society of Microbiology Conference, May 2001, Abstract No. C-443.

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ISU is best known for its degree programs in science, engineering, and agriculture. ISU is also home of the world's first electronic digital computing device, the Atanasoff–Berry Computer.
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(28.) Boyce WM, Asai DJ, Wilder JK, Kazacos KR. Physicochemical physicochemical /phys·i·co·chem·i·cal/ (fiz?i-ko-kem´ik-il) pertaining to both physics and chemistry.

phys·i·co·chem·i·cal
adj.
1. Relating to both physical and chemical properties.
 characterization and monoclonal and polyclonal antibody recognition of Baylisascaris procyonis larval excretory-secretory antigens. J Parasitol 1989;75:540-8.

(29.) Boyce WM, Branstetter BA, Kazacos KR. Comparative analysis of larval excretory-secretory antigens of Baylisascaris procyonis, Toxocara canis and Ascaris suum by Western blotting and enzyme immunoassay. Int J Parasitol 1988;18:109-13.

(30.) Gass JDM, Gilbert WR, Guerry RK, Scelfo R. Diffuse unilateral subacute neuroretinitis. Opthalmology 1978:85:521-45.

(31.) Anderson DC, Greenwood R, Fishman M, Kagan IG. Acute infantile hemiplegia hemiplegia /hemi·ple·gia/ (-ple´jah) paralysis of one side of the body.hemiple´gic

alternate hemiplegia  paralysis of one side of the face and the opposite side of the body.
 with cerebrospinal fluid eosinophilic pleocytosis pleocytosis /pleo·cy·to·sis/ (ple?o-si-to´sis) presence of a greater than normal number of cells in cerebrospinal fluid.

ple·o·cy·to·sis
n.
: an unusual case of visceral larva migrans. J Pediatr 1975;86:247-9.

(32.) Jacobson JE, Kazacos KR, Montague FH. Prevalence of eggs of Baylisascaris procyonis (Nematoda:Ascaroidea) in raccoon scats from an urban and a rural community. J Wildl Dis 1982;18:461-4.

(33.) Henderson DA. The looming threat of bioterrism. Science 1999;283:1279-82.

(34.) Phills JA, Harrold AJ, Whiteman GV, Perelmutter L. Pulmonary infiltrates, asthma and eosinophilia due to Ascaris suum infestation infestation /in·fes·ta·tion/ (-fes-ta´shun) parasitic attack or subsistence on the skin and/or its appendages, as by insects, mites, or ticks; sometimes used to denote parasitic invasion of the organs and tissues, as by helminths.  in man. N Engl J Med 1972;286:965-70.

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Address for correspondence: Frank Sorvillo, UCLA School of Public Health, Box 951772, Los Angeles, CA 90024, USA; fax: 714-816-9099; e-mail: fsorvill@ucla UCLA University of California at Los Angeles
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Frank Sorvillo, * Lawrence R. Ash, * O.G.W. Berlin, * ([dagger]) JoAnne Yatabe, ([dagger]) Chris Degiorgio, ([double dagger]) and Stephen A. Morse ([section])

* University of California The University of California has a combined student body of more than 191,000 students, over 1,340,000 living alumni, and a combined systemwide and campus endowment of just over $7.3 billion (8th largest in the United States).  Los Angeles School The Los Angeles School of Urbanism is an academic movement emerged during the mid-1980s, loosely based at the University of Southern California and UCLA, that poses a challenge to the dominant Chicago School of Urbanism.  of Public Health, Los Angeles, California; ([dagger]) Specialty Labs, Santa Monica, California For other uses, see Santa Monica (disambiguation).
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Author:Morse, Stephen A.
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Date:Apr 1, 2002
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Remote Sensing and Geographic Information Systems in Epidemiology.
Reassessment of the allegheny woodrat (Neotoma magister) in Indiana.
Raccoon roundworm eggs near homes and risk for larva migrans disease, California communities.
Baylisascaris procyonis in the metropolitan Atlanta area.
Baylisascaris procyonis in California.
Wildlife as source of zoonotic infections.
International attention for zoonotic infections.
Wildlife, exotic pets, and emerging zoonoses (1).
Thermal death point of Baylisascaris procyonis eggs.(LETTERS)(Letter to the editor)

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