First Detection and Genotyping of Human-Associated Microsporidia in Pigeons from Urban Parks

Abstract

Microsporidia are ubiquitous opportunistic parasites in nature infecting all animal phyla, and the zoonotic potential of this parasitosis is under discussion. Fecal samples from 124 pigeons from seven parks of Murcia (Spain) were analyzed. Thirty-six of them (29.0%) showed structures compatible with microsporidia spores by staining methods. The DNA isolated from 26 fecal samples (20.9%) of microsporidia-positive pigeons was amplified with specific primers for the four most frequent human microsporidia. Twelve pigeons were positive for only Enterocytozoon bieneusi (9.7%), 5 for Encephalitozoon intestinalis (4%), and one for Encephalitozoon hellem (0.8%). Coinfections were detected in eight additional pigeons: E. bieneusi and E. hellem were detected in six animals (4.8%); E. bieneusi was associated with E. intestinalis in one case (0.8%); and E. hellem and E. intestinalis coexisted in one pigeon. No positive samples for Encephalitozoon cuniculi were detected. The internally transcribed spacer genotype could be completed for one E. hellem-positive pigeon; the result was identical to the genotype A1 previously characterized in an E. hellem Spanish strain of human origin. To our knowledge, this is the first time that human-related microsporidia have been identified in urban park pigeons. Moreover, we can conclude that there is no barrier to microsporidia transmission between park pigeons and humans for E. intestinalis and E. hellem. This study is of environmental and sanitary interest, because children and elderly people constitute the main visitors of parks and they are populations at risk for microsporidiosis. It should also contribute to the better design of appropriate prophylactic measures for populations at risk for opportunistic infections.Microsporidia are intracellular obligate parasites mainly considered as opportunistic pathogens (58), ubiquitous in nature, infecting all animal phyla (6, 59). Although initially associated with AIDS patients, they are being detected in increasing numbers in immunocompetent patients and thus are gaining attention as emerging pathogens (25,33,35,53,56). The phylum Microsporidia contains over 144 genera and 1,200 species (59). The number of genera implicated in human microsporidiosis has increased at the same rate as the improvements in diagnostic techniques, and the interest in this group of parasites has grown accordingly. To date, eight genera are recognized as human pathogens: Nosema, Vittaforma, Pleistophora, Encephalitozoon, Enterocytozoon, Brachiola, Trachipleistophora, and Microsporidium. Among these, Enterocytozoon bieneusi is the species of microsporidia that most frequently causes infection in humans, followed by Encephalitozoon intestinalis, Encephalitozoon hellem, and Encephalitozoon cuniculi.

Enterocytozoon bieneusiin human and animals, focus on laboratory identification and molecular epidemiology

“…Is man a natural reservoir for the parasite or an accidental host in whom the infection becomes possible because of the deterioration of his immune system? For instance, after being identified in humans, spores of E. bieneusi were detected in numerous animal species, especially mammals but also birds, and in environmental source such as surface water, swimming pools or rivers (Coupe et al, 2006;Dowd et al, 1998;Fournier et al, 2000;Haro et al, 2006;Haro et al, 2005;Santin et al, 2004;Sparfel et al, 1997). Analysis of the sequence of the 243-bp internal transcribed spacer rRNA gene has revealed a considerable genetic variation within E. bieneusi isolates of human and animal origins.…”

“…While early investigation revealed that coccidian parasites were a leading cause of chronic diarrhoea in AIDS patients, the development of improved microscopic, immunological and al., 1985). The development of new tools for diagnosis and especially molecular methods have shown that E. bieneusi was present in a large number of domestic and wild mammals as well as birds (Haro et al, 2006;Haro et al, 2005;Kondova et al, 1998;and reviewed in Mathis et al, 2005). Thanks to molecular methods again, the potential of zoonotic transmission was quickly supported by phylogenetic studies showing that several genotypes can infect humans as well as animals (Curry, 1999;Dengjel et al, 2001;Drosten et al, 2005;Lobo et al, 2006a;Santin et al, 2006;Sulaiman et al, 2003a;Sulaiman et al, 2003b;Sulaiman et al, 2004).…”

Occurrence of Cryptosporidium hominis in pigeons (Columba livia)

“…The most common species of pigeon in the Canary Islands is Columba livia which inhabits forests, cities and villages (Emmerson 1985). This species can transmit microorganisms to humans that could be pathogenic as is the case of Cryptococcus neoformans (Emmons 1951(Emmons , 1955Kwon-Chung and Bennett 1978) or, more recently, Enterocytozoon bieneusi and Encephalitozoon intestinalis (Haro et al 2005). On the other hand, it is known that some birds can acquire C. hominis oocysts from local garbage and other unhygienic places (Graczyk et al 2008), as it could be wastewater.…”

“…Elderly people and children are at a higher risk to come in close contact with pigeons in gardens and public parks (Haro et al 2005). The most common species of pigeon in the Canary Islands is Columba livia which inhabits forests, cities and villages (Emmerson 1985).…”

Transmission of Enterocytozoon bieneusi between a Child and Guinea Pigs

“…Enterocytozoon bieneusi has been reported to occur in several species of domestic and wild animals, including dogs, cats, pigs, and cattle (3). Recent surveys found that pigs and park pigeons had genotypes of E. bieneusi that were potentially infectious to humans (2,10). Cattle in the United States and other countries were primarily infected with host-specific E. bieneusi but also carried some genotypes previously found in humans, and thus the infection was potentially zoonotic (17,19).…”