Microsporidian Species Known To Infect Humans Are Present in Aquatic Birds: Implications for Transmission via Water?

Abstract

Human microsporidiosis, a serious disease of immunocompetent and immunosuppressed people, can be due to zoonotic and environmental transmission of microsporidian spores. A survey utilizing conventional and molecular techniques for examining feces from 570 free-ranging, captive, and livestock birds demonstrated that 21 animals shed microsporidian spores of species known to infect humans, including Encephalitozoon hellem (20 birds; 3.5%) and Encephalitozoon intestinalis (1 bird; 0.2%). Of 11 avian species that shed E. hellem and E. intestinalis, 8 were aquatic birds (i.e., common waterfowl). The prevalence of microsporidian infections in waterfowl (8.6%) was significantly higher than the prevalence of microsporidian infections in other birds (1.1%) (P < 0.03); waterfowl fecal droppings contained significantly more spores (mean, 3.6 ؋ 10 5 spores/g) than nonaquatic bird droppings contained (mean, 4.4 ؋ 10 4 spores/g) (P < 0.003); and the presence of microsporidian spores of species known to infect humans in fecal samples was statistically associated with the aquatic status of the avian host (P < 0.001). We demonstrated that a single visit of a waterfowl flock can introduce into the surface water approximately 9.1 ؋ 10 8 microsporidian spores of species known to infect humans. Our findings demonstrate that waterborne microsporidian spores of species that infect people can originate from common waterfowl, which usually occur in large numbers and have unlimited access to surface waters, including waters used for production of drinking water.Microsporidians are obligate intracellular parasites that are emerging opportunistic pathogens that infect both immunocompromised and immunocompetent people (41,42,43). Microsporidians are on the Contaminant Candidate List of the U.S. Environmental Protection Agency because their transmission routes are unknown, spore identification, removal, and inactivation in drinking water are technologically challenging (27), and human infections are difficult to treat (11). Considerable evidence gathered to date indicates that water is involved in the epidemiology of human microsporidiosis (10,12,14,15,25,35,38); however, this epidemiological link has not been proved conclusively (16). Identification of microsporidian spores of species known to infect humans (Encephalitozoon intestinalis, Encephalitozoon hellem, Encephalitozoon cuniculi, and Enterocytozoon bieneusi)is a challenge because microsporidians can infect a variety of nonhuman hosts and spore morphology does not provide enough information for species identification (39). This challenge is met by the multiplex fluorescence in situ hybridization (FISH) assay, which employs fluorescently labeled oligonucleotide probes targeted to species-specific sequences of 18S rRNA (19,20,22). By using various fluorochromes to label different oligonucleotide probes, spores of E. intestinalis, E. hellem, E. cuniculi, and E. bieneusi are stained red, green, orange, and yellow, respectively (19,20,22).E. hellem has been found most frequently in avian ho...

Molecular Epidemiologic Characterization of Enterocytozoon bieneusi in HIV-Infected Persons in Benin City, Nigeria

“…Of the six known genotypes, three have been reported from studies in other African countries. 20,21 Genotypes A (28.5%) and CAF2 (2.5%) were slightly lower in prevalence than the genotypes reported in Cameroon (40.0%) 18 and Gabon (6.6%), 19 whereas genotype D (40.2%) had a higher prevalence than the genotype (15.0%) observed in Cameroon. 18 Both genotypes D and IV have a broad host and geographic range.…”

“…These individuals are more likely to have non-vocational jobs that may expose them to bodies of water and animals, which are known sources of microsporidial infections. 18,19 HIV patients that used streams and rivers as sources of water had significantly (P = 0.011) higher prevalence of microsporidial infections. Bodies of water are known sources of microsporidial infection.…”

“…Bodies of water are known sources of microsporidial infection. 6,14,19 These bodies of water are used as sources for drinking and domestic use, thereby increasing the chances of E. bieneusi infection. Surprisingly, animal contact was not a risk factor for microsporidiosis in this study.…”

Molecular markers and sentinel organisms for environmental monitoring

“…Microsporidia infects a variety of vertebrate and invertebrate hosts, and approximately 14 species have been reported to infect people. Of these E. intestinalis and E. bieneusi have been reported to be zoonotic and to infect domestic animals and livestock (Slodkowicz-Kowalska et al, 2006). Although the actual transmission route of this specific spore species is not known, it is quite possible that infectious spores of human or animal origin passed to the aquatic environments via feces or urine (Graczyk et al, 2004).…”

Retrospective Species Identification of Microsporidian Spores in Diarrheic Fecal Samples from Human Immunodeficiency Virus/AIDS Patients by Multiplexed Fluorescence In Situ Hybridization

“…The fluorescence in situ hybridization (FISH) assay uses fluorescently labeled 19-bp oligonucleotide probes targeted to microsporidium species-specific sequences of 16S rRNA; therefore, spore identification is species specific (18,19,21,31). The FISH assay was originally developed for E. hellem (21); however, alignment of the respective 16S rRNA regions of 22 other species of microsporidia (21) allowed the design of oligonucleotide probes specific to E. intestinalis (18) and to E. bieneusi and E. cuniculi (19).…”