Yeasts and yeast-like fungi

Public Health Significance of Urban Pests Birds 255 254 thropic wild avian samples from excretions, the intestinal tract and other organs: Candida guilliermondii , Candida krusei, Candida tropicalis, Candida pseudotropicalis and Candida parapsilosis Frágner, 1962; Kawakita van Uden, 1965; Schönborn, Schütze Pöhler, 1969; Cragg Clayton, 1971; Kocan Hasenclever, 1972; Monga, 1972; Gugnani, Sandhu Shome, 1976; Guiguen, Boisseau-Lebreuill Couprie, 1986; Pinowski, Kavanagh Górski, 1991; Hubálek, 1994; Haag-Wackernagel Moch, 2004. An outb- reak of peritonitis due to C. parapsilosis in 12 patients undergoing peritoneal dialysis was attributed to contaminated pigeon excreta on window sills Greaves et al., 1992. 8.2.3.1.2. Crypotococcus Avian especially feral pigeon excretions represent a significant natural source of crypto- coccosis in people. The first isolation of C. neoformans its teleomorph stage is Filobasidiella neoformans , a basidomycetous yeast from the nests and droppings of feral pigeons Emmons, 1955, 1960 was followed by a number of similar reports worldwide Yamamoto, Ishida Sato, 1957; Littman Schneierson, 1959; Frágner, 1962; Tsubura, 1962; Bergman, 1963; Muchmore et al., 1963; Silva Paula, 1963; Frey Durie, 1964; Partridge Winner, 1965; Procknow et al., 1965; Randhawa, Clayton Riddell, 1965; Taylor Duangmani, 1968; Hubálek, 1975; Gugnani, Sandhu Shome, 1976; Refai et al., 1983; Ruiz, Vélez Fromtling, 1989; Yildiran et al., 1998; Haag-Wackernagel Moch, 2004; Chee Lee, 2005. The association between C. neoformans var. grubii formerly C. neoformansserotype A and the feral pigeon is remarkable Denton Di Salvo, 1968, whereas the occurrence of the fungus in faeces of other wild bird species is surprisingly scarce. As many as a hundred thousand to a million viable C. neoformans cells have been detected per gram of pigeon exc- reta in different parts of the world Emmons, 1960; Hubálek, 1975; Ruiz, Fromtling Bulmer, 1981; Ruiz, Neilson Bulmer, 1982; Ruiz, Vélez Fromtling, 1989. This association was shown to be conditioned nutritionally, due to the ability of the yeast- like organism to utilize all basic low-molecular-weight nitrogenous substances from avian urine – that is, uric acid, creatinine, xanthine, guanine and urea – and due to the tena- city of the causative agent, C. neoformansStaib, 1962, 1963; Walter Yee, 1968; Hubálek, 1975; Ruiz, Neilson Bulmer, 1982. The birds pigeons serve therefore largely as a les- sor Hubálek, Juˇricová Halouzka, 1995 for the fungus. However, carriage of the fun- gus has also been proved by isolating it from the feet and bills of feral pigeons Littman Borok, 1968 or from their lower and upper digestive tracts Sethi Randhawa, 1968; Swinne-Desgain, 1976; Khan et al., 1978; Guiguen, Boisseau-Lebreuill Couprie, 1986; Rosario et al., 2005. In an experiment, pigeons with C. neoformans administered into the crop excreted the fungus sporadically in faeces up to 22 days, but harboured it for at least 86 days in the crop Swinne-Desgain, 1976; this study demonstrated that pigeons could carry the fungus in their upper digestive tract. Spontaneous natural cryptococcosis has only rarely been observed in feral columbiforms Hermoso de Mendoza et al., 1984. The course of experimental avian infections is usually abortive; only intracerebral inoculation was sufficient to cause death in some pigeons; the agent persisted in the brain for up to 11 weeks Littman, Borok Dalton, 1965; Böhm et al., 1974. The low susceptibility of birds to cryptococcosis may be due to the poor or nil growth of the fungus at 41°C – that is, at the avian body temperature. Mycobacterium avium was also isolated from a collared dove Volner, 1978; in experi- ments, this dove species was found to be much less susceptible than the chickens, but could be a potential carrier of the infectious agent Rossi, 1969; Hejlíˇcek Treml, 1993b. Mycobacteria, including M. avium-intracellulare complex, were detected in 19 of 153 faecal samples of feral pigeons collected in Japan Tanaka et al., 2005. However, biolo- gical and molecular typing sometimes even nucleotide sequencing of M. avium strains from free-living birds seems to be necessary for a proper epidemiological evaluation of the birds as sources of human infections – that is, to compare the avian and clinical human isolates closely and to detect whether they are identical or not Schaeffer et al., 1973; McFadden et al., 1992. Also, there are a few unconfirmed, anecdotal cases of M. avium clinical infections of people ornithologists who collected and examined urban owl and raptor pellets. Mycobacterium xenopi was occasionally found to cause human disease – for example, a nosocomial outbreak in Le Havre, France, where 558 cases were diagnosed for the per- iod 1965–1967; free-living birds were the probable source of the outbreak, and the cau- sative agent was isolated from droppings of local tree sparrows and common blackbirds Joubert, Desbordes-Lize Viallier, 1971. Other mycobacteria potentially pathogenic to people M. avium-intracellulare, M. aquae, M. flavescens and M. fortuitum were isolated from rooks Kubín Matˇejka, 1967, anatids Schaefer et al., 1973, gulls and jackdaws with necrosis in the liver and spleen Smit et al., 1987.

8.2.3. Fungi

8.2.3.1. Yeasts and yeast-like fungi

8.2.3.1.1. Candida Candidosis also called candidiasis and moniliasis is, after aspergillosis, the second most significant mycosis of domestic and captive birds. In wild birds, however, the disease is virtually unknown, although C. albicans has often been isolated from the gastrointestinal tract and excretions of gulls Kawakita van Uden, 1965; Cragg Clayton, 1971; Buck, 1983, 1990, pigeons and other wild birds Littman Schneierson, 1959; Frágner, 1962; Partridge Winner, 1965; Brandsberg et al., 1969; Schönborn, Schütze Pöhler, 1969; Kocan Hasenclever, 1974; Hasenclever Kocan, 1975; Gugnani, Sandhu Shome, 1976; Refai et al., 1983; Pinowski, Kavanagh Górski, 1991; Hubálek, 1994; Haag- Wackernagel Moch, 2004, as well as from pellets of synanthropic rooks, nests of col- lared doves and feathers of house sparrows Hubálek, 1994. Candida albicans seems to be especially frequent in fresh droppings of gulls: it was recovered from about half of the samples tested along the eastern coastline of the United States Buck, 1983, 1990. Experimental observations of a gull fed fish containing C. albicans demonstrated a heavy shedding of the yeast via faeces for the next 13 days, and even 40 days post-feeding the gull excreted the yeast sporadically, even though it was treated with ketoconazole Buck, 1986. The gulls may thus serve as carriers of C. albicansor as a reservoir for it. However, no C. albicans infections of people have been reported as attributable to, or directly asso- ciated with, urban birds. Other Candida spp. pathogenic to people have been isolated from a number of synan- Public Health Significance of Urban Pests Birds 257 256 Contaminated areas could pose a human health hazard for a prolonged period of time Latham et al., 1980. For example, the endemic reactivity of children from a school in the United States to the skin-test antigen histoplasmin was ascribed to the presence of a nearby roosting site of blackbirds, the soil of which was the source of H. capsulatum Dodge, Ajello Engelke, 1965. Major outbreaks of histoplasmosis 300 human cases occurred in Mason City, Iowa, following two repeated clearings in 1962 and 1964 of a park area where large numbers of starlings had been roosting for years D’Alessio et al., 1965; Tosh et al., 1966. A total of 355 students showed symptoms of histoplasmosis after the soil was rototilled in an Indiana school courtyard known as a blackbird–starling roos- ting site; H. capsulatum was then also isolated from filters in the school air-conditioning system Chamany et al., 2004. In another case, children were infected through contact with a nesting place of common grackles, contaminated with the fungus. Also, a great number of people working on a ring-billed gull Larus delawarensis nesting colony site in winter developed acute pulmonary histoplasmosis, and H. capsulatum was isolated from the nesting site Waldman et al., 1983.

8.2.4. Protozoa