Resumen de Prevalence of Alaria infection in companion animals in north central Oklahoma from 2006 through 2015 and detection in wildlife
Eileen M. Johnson, Yoko Nagamori, Rebecca A. Duncan Decocq, Patrick N. Whitley, Akhilesh Ramachandran, Mason V. Reichard
OBJECTIVE To determine the prevalence of Alaria infection in cats and dogs in north central Oklahoma over various periods and investigate whether wild animal species in this region were also infected.
DESIGN Combined cross-sectional study and case series.
SAMPLE Results of parasitological testing of fecal samples from 5,417 client-owned dogs and 1,246 client-owned cats (2006 through 2014); fecal samples from 837 shelter or rescue dogs and 331 shelter or rescue cats (2013 and 2014) and 268 feral cats (2015); tongue or jowl samples from cadavers of 43 wild pigs, 3 opossums, and 1 raccoon; and intestinal tract segments from cadavers of 48 cats and 5 coyotes.
PROCEDURES Various parasite recovery techniques were performed to detect various Alaria stages in samples. Recovered adult trematodes and mesocercariae were used for PCR assay and sequencing of the 28S rRNA gene.
RESULTS Prevalence of Alaria infection was significantly higher in feral cats (9.0%) than in shelter or rescue cats (0.6%) and client-owned cats (1.4%) and in shelter or rescue dogs (1.8%) than in client-owned dogs (0.2%). Mesocercariae were recovered from tissue samples from 11 (26%) wild pigs and 1 opossum. Amplicon sequences from adult trematodes and mesocercariae were 100% identical to each other and 99% homologous to GenBank sequences of Alaria alata and Alaria mustelae.
CONCLUSIONS AND CLINICAL RELEVANCE Prevalence of Alaria infection in the study area has increased in dogs and cats since 1990, when infections were rare. Prevalence in wild pigs was similar to that in Eurasia, where A alata is considered an emerging zoonotic parasite.
Diplostomatid trematodes in the genus Alaria have a worldwide distribution. Domestic and wild carnivores are the definitive hosts.1–6 Adult trematodes in the small intestine pass eggs in the feces, and the eggs embryonate and hatch in fresh water. Newly hatched miracidiae penetrate susceptible species of fresh water snails (eg, Helistoma, Planorbis, Lymnea, and Anisus spp) that support asexual development of miracidiae into sporocysts and furcocercous cercariae.1,2,6,7 Cercariae penetrate the skin of tadpoles or frogs and become mesocercariae.1,2,8 Various species of birds, reptiles, and mammals (including humans) that ingest the infected frogs can serve as collector (paratenic) hosts.1,2,6,9–13 Carnivores become infected when they ingest infected frogs or paratenic hosts or through transmammary transmission.1–6 The mesocercariae migrate to the lungs and encyst as metacercariae that are coughed up and swallowed. Recognized Alaria spp include Alaria alata, Alaria mustelae, Alaria canis, Alaria arisaemoides, Alaria intermedia, Alaria taxidae, and Alaria marcianae.6 In reported cases of human alariosis in North America, Alaria infection was acquired through consumption of improperly cooked game meat.9,10 The only Alaria sp recorded to date in Europe is A alata.1,6,13,14 Although not definitively associated with human disease, A alata has been experimentally transmitted to a rhesus monkey.11,13 Over the past decade during mandatory testing of wild pigs (Sus scrofa scrofa) for Trichinella spp in the European Union, A alata mesocercariae have been discovered in wild pig tissues, primarily in muscle fascia and adipose tissue.1,6,14–19 In Europe, alariosis had been classified as a low-risk zoonosis.1,6,13,14 However, with expansion of wild pig populations, an increase in the prevalence of mesocercariae in wild pigs, an increase in human consumption of meat from wild pigs, changes in cooking methods, and recognition of severe and fatal disease in humans, A alata is now considered an emerging threat to human health.1,6,14–20 Surveillance of Trichinella spp in the United States is not mandatory and does not include wild pig populations.21 Control has been achieved in domesticated pigs (Sus scrofa domesticus) through enforcement of laws that prevent feeding of raw garbage and through improvements in biosecurity and hygiene in confinement-type swine production units. Serologic testing (ELISA) is used in swine production herds to determine Trichinella status. No information is available on the role of wild pigs as a source of human infection with Alaria mesocercariae in the United States.
Efforts to control expanding wild pig populations in the United States through regulated hunting and trapping have been unsuccessful.22,23 This population expansion is believed to be due to periodic release of wild pigs from Eurasia into different areas of the United States for hunting and the escape of domesticated pigs that subsequently interbreed with these released wild pigs.22,23 Adaptability of wild pigs is related to their omnivorous feeding habits, high reproductive potential, intelligence, and reclusive nature. They are considered large game and are used for hunting purposes and human consumption in many parts of the world.20,24 Studies1,6,13,18,25 in Europe have revealed a high prevalence of A alata infection in red fox and wolf populations, which are also believed to be expanding. In North America, most reports4,5,26–32 of Alaria infections in domesticated and wild carnivores pertain to Canada, the northern United States, and Florida. In a study33 of endoparasitism in client-owned dogs conducted in north central Oklahoma from 1981 through 1990, no Alaria ova were detected in 12,515 fecal samples. The purpose of the study reported here was to obtain an updated estimate of the prevalence of Alaria infection in various dog and cat populations and to determine whether infection existed in wildlife reservoir hosts, primarily wild pigs, in north central Oklahoma.
