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Revista Brasileira de Parasitologia Veterinária

Print version ISSN 0103-846XOn-line version ISSN 1984-2961

Rev. Bras. Parasitol. Vet. vol.24 no.3 Jaboticabal July/Sept. 2015

http://dx.doi.org/10.1590/S1984-29612015063 

Review Article

Cryptosporidium infections in birds - a review

Infecção por Cryptosporidium em aves - uma revisão

Alex Akira Nakamura 1  

Marcelo Vasconcelos Meireles 1   *  

1Faculdade de Medicina Veterinária, Universidade Estadual Paulista – UNESP, Campus de Araçatuba, Araçatuba, SP, Brasil

ABSTRACT

Cryptosporidiosis is one of the main protozoan infections in birds. It manifests as either a respiratory or a digestive illness, and it affects a very large number of avian species across several continents. The aim of this review is to report on the main results of studies on cryptosporidiosis among birds and the importance of these results to veterinary medicine and public health.

Key words: Cryptosporidium spp.; wild birds; poultry

RESUMO

A criptosporidiose constitui-se em uma das principais infecções por protozoários em aves, manifestando-se como enfermidade respiratória ou digestiva, em dezenas de espécies aviárias, em vários continentes. O objetivo desse trabalho foi relatar, por meio de revisão de literatura, os principais resultados de estudos sobre criptosporidiose em aves e sua importância para a medicina veterinária e saúde pública.

Palavras-Chave: Cryptosporidium spp.; aves selvagens; aves domésticas

Introduction

Protozoa of the genus Cryptosporidium parasitize fish, amphibians, reptiles, birds and mammals. Protozoan biological cycles take place on the surface of the epithelial cells in the gastrointestinal and respiratory tracts, in the bursa of Fabricius, and, less frequently, in other organs (CURRENT et al., 1986; BARTA & THOMPSON, 2006; VALIGUROVÁ et al., 2008), causing clinical and subclinical infections (SANTÍN, 2013).

The first description of Cryptosporidium infection among birds was reported by Tyzzer (1929) and involved the cecal epithelium of chicken. Slavin (1955)described a new species of Cryptosporidium that was causing mortality among young turkeys and suggested the name Cryptosporidium meleagridis. Nearly two decades later, cryptosporidiosis was diagnosed among domestic geese (Anser anser) (PROCTOR & KEMP, 1974) and broiler chickens (FLETCHER et al., 1975). Current et al. (1986) described the biological cycle of Cryptosporidium in domestic chickens and named the species Cryptosporidium baileyi. The third valid species of this parasite, Cryptosporidium galli, was described by Pavlásek (1999) from the proventriculi of chickens and was later revised by Ryan et al. (2003a).

Cryptosporidiosis is one of the main protozoan infections among birds. It manifests as either a respiratory or a digestive disease, and it affects a very large number of avian species across all continents except Antarctica (Table 1). Various aspects of cryptosporidiosis among humans and animals have been addressed (RAMIREZ et al., 2004; XIAO et al., 2004; JEX et al., 2008; BOWMAN & LUCIO-FORSTER, 2010; RYAN, 2010), but the literature regarding the occurrence of Cryptosporidium infection among avian species is demonstrably sparse.

Table 1 Cryptosporidium species and genotypes identified in birds using molecular diagnostic techniques. 

Species/genotype Host Order Site of infection Gene target Geographic origin Reference
Cryptosporidium baileyi Anseriformes, Cathartiformes, Charadriiformes, Columbiformes, Falconiformes, Galliformes, Gruiformes, Passeriformes, Piciformes, Psittaciformes, Strigiformes, Struthioniformes Bursa of Fabricius, conjunctiva, kidneys, respiratory tract, cloaca, rectum 18S rRNA, Actin, HSP-70, COWP Africa, Asia, Europe, North America, South America Morgan et al. (2001), Ryan et al. (2003b), Chvala et al. (2006), Ng et al. (2006), Huber et al. (2007), Van Zeeland et al. (2008), Nakamura et al. (2009), Molina-López et al. (2010), Sevá et al. (2011), Qi et al. (2011), Wang et al. (2011), Coldwell et al. (2012), Schulze et al. (2012), Wang et al. (2012), Baroudi et al. (2013), Bougiouklis et al. (2013), Nakamura et al. (2014), Qi et al. (2014), Wang et al. (2014b), Li et al. (2015), Máca & Pavlásek (2015)
Cryptosporidium meleagridis Columbiformes, Galliformes, Passeriformes, Psittaciformes Small intestine, large intestine 18S rRNA, Actin, HSP-70, COWP, GP60 Africa, Asia, Europe, Oceania, North America, South America Morgan et al. (2000), Morgan et al. (2001), Ryan et al. (2003b), Huber et al. (2007), Pagès-Manté et al. (2007), Nakamura et al. (2009), Qi et al. (2011), Silverlås et al. (2012), Wang et al. (2012), Baroudi et al. (2013), Wang et al. (2014b), Li et al. (2015), Máca & Pavlásek (2015), Reboredo-Fernández et al. (2015)
Cryptosporidium galli Bucerotiformes, Galliformes, Passeriformes, Psittaciformes, Phoenicopteriformes Proventriculus 18S rRNA, Actin, HSP-70 Asia, Europe, Oceania, South America Ryan et al. (2003a), Ng et al. (2006), Antunes et al. (2008), Nakamura et al. (2009), Silva et al. (2010), Sevá et al. (2011), Qi et al. (2011), Nakamura et al. (2014)
Avian genotype I Galliformes, Passeriformes nd 18S rRNA, Actin Oceania, South America Ng et al. (2006), Nakamura et al. (2009)
Avian genotype II Galliformes, Psittaciformes, Struthioniformes, Cloaca, rectum, bursa of Fabricius 18S rRNA, Actin, HSP-70 Asia, Oceania, South America Santos et al. (2005), Meireles et al. (2006), Ng et al. (2006), Nakamura et al. (2009), Sevá et al. (2011), Nguyen et al. (2013), Wang et al. (2014b)
Avian genotype III Passeriformes, Psittaciformes, Proventriculus 18S rRNA, Actin, HSP-70, COWP Asia, Oceania, North America, South America Abe & Makino (2010), Ng et al. (2006), Nakamura et al. (2009), Makino et al. (2010), Qi et al. (2011), Gomes et al. (2012), Nakamura et al. (2014), Ravich et al. (2014)
Avian genotype IV Psittaciformes nd 18S rRNA Europe Ng et al. (2006)
Avian genotype V Psittaciformes nd 18S rRNA, actin, HSP-70 Asia, South America Abe & Makino (2010), Qi et al. (2011), Nakamura et al. (2014)
Goose genotypes I-V Anserifornes nd 18S rRNA North America Jellison et al. (2004), Zhou et al. (2004)
Black duck genotype Anseriformes nd 18S rRNA Oceania Morgan et al. (2001)
Eurasian Woodcock genotype Charadriiformes Proventriculus 18S rRNA, HSP-70 Europe Ryan et al. (2003b)
Cryptosporidium andersoni Galliformes nd 18S rRNA, Actin Europe Ng et al. (2006)
Cryptosporidium muris Caprimulgiformes, Struthioniformes nd 18S rRNA, HSP-70, Actin Asia, Europe Ng et al. (2006), Qi et al. (2014)
Cryptosporidium parvum Accipitriformes, Anseriformes, Charadriiformes, Galliformes, Passeriformes, Psittaciformes Small intestine, caecum TRAP-C2, beta-tubulin,18S rRNA, COWP Asia, Europe, North America, South America Graczyk et al. (1998), Zhou et al. (2004), Zylan et al. (2008), McEvoy & Giddings (2009), Nakamura et al. (2009), Gomes et al. (2012), Reboredo-Fernández et al. (2015)
Cryptosporidium hominis Anseriformes nd 18S rRNA North America Zhou et al. (2004)

nd: the site of infection was not reported.

The objective of the present study was to report on the main results of studies on cryptosporidiosis among birds and the importance of these results to veterinarian medicine and public health by reviewing the literature.

Etiological Agent and Host Specificity

Cryptosporidium spp. are parasites classified as members of the phylum Apicomplexa, class Sporozoea, subclass Coccidia, order Eucoccidiida and family Cryptosporidiidae, which contains a single genus, Cryptosporidium (FAYER, 2008). However, there is evidence that the genus Cryptosporidium might be more closely related to the Gregarinia than to the Coccidia (BARTA & THOMPSON, 2006; CAVALIER-SMITH, 2014).

The classification of species within the genus Cryptosporidium is constantly being updated using molecular methods and data on morphology, biology and host specificity. There are descriptions of 27 to 30 different species of Cryptosporidium, although there is still some debate regarding which species are valid (ŠLAPETA, 2013; RYAN & HIJJAWI, 2015).

In birds, three species of Cryptosporidium have been reported, including C. baileyi, C. galli and C. meleagridis. Many genotypes have also been described, mainly based on molecular data (SMITH et al., 2007; XIAO & FAYER, 2008; XIAO & FENG, 2008; RYAN et al., 2014). The lack of biological, morphological or host specificity data has prevented the naming of new species related to Cryptosporidium avian genotypes (FAYER, 2010).

Cryptosporidium baileyi is the species most frequently diagnosed among birds, with reports of clinical or subclinical disease in 12 avian orders. Moreover, this is the most frequent species among the order Galliformes. Cryptosporidium galli has been found in several species of five different orders of birds, most frequently among Passeriformes and Psittaciformes, whereas C. meleagridis has been detected in four orders of birds, with infection occurring preferentially among the Galliformes (Table 1). Cryptosporidium meleagridis is the only avian species that infects mammals, and both natural and experimental infections have been reported (DARABUS, 1997; SRÉTER et al., 2000; AKIYOSHI et al., 2003; DARABUS & OLARIU, 2003).

Avian genotypes I, II, III, IV and V have been reported in birds (SANTOS et al., 2005; MEIRELES et al., 2006; NG et al., 2006; ABE & MAKINO, 2010), as have five goose genotypes (JELLISON et al., 2004; ZHOU et al., 2004), the black duck genotype and the Eurasian woodcock genotype (MORGAN et al., 2001) (Table 1).

There is still little information on the host specificity of the Cryptosporidium avian genotypes (Table 1). Avian genotype I has been found in canaries (Serinus canaria) and Indian peafowl (Pavo cristatus) (NG et al., 2006; NAKAMURA et al., 2009), whereas the presence of avian genotype III has been reported in several species of Psittaciformes and Passeriformes (NG et al., 2006; NAKAMURA et al., 2009; MAKINO et al., 2010; QI et al., 2011; GOMES et al., 2012; NAKAMURA et al., 2014).

The avian genotype II has been described in ostriches and in several Psittaciformes species (SANTOS et al., 2005; MEIRELES et al., 2006; NG et al., 2006; SEVÁ et al., 2011; NGUYEN et al., 2013). Although Wang et al. (2014b) reported the presence of avian genotype II in 0.78% (3/385) of fecal samples from chickens in China, Meireles et al. (2006) did not observe infection among chickens that were experimentally infected with avian genotype II and screened for Cryptosporidium infection using cytology, histology and oocyst screening in feces.

Infections by avian genotype IV and the Eurasian woodcock genotype have only been described once each: in the Japanese white-eye (Zosterops japonicus) and the Eurasian woodcock (Scolopax rusticola), respectively (NG et al., 2006). Regarding avian genotype V, which was first described by Abe & Makino (2010) among cockatiels (Nymphicus hollandicus), there have been two additional reports among birds of the order Psittaciformes (QI et al., 2011; NAKAMURA et al., 2014) and one report in reptiles (Iguana iguana) (KIK et al., 2011). The black duck genotype and the geese genotypes I to V have been described in the order Anseriformes and seem to have a narrower spectrum of hosts (JELLISON et al., 2004; ZHOU et al., 2004).

The infectivity of C. parvum to domestic chickens was assessed by Lindsay et al. (1987a) and Palkovič & Maroušek (1989), who observed clinical signs after intratracheal inoculation with oocysts. However, parasite colonization was found to be restricted to the respiratory tract, and low numbers of oocysts were produced. Cryptosporidium species that are more common among mammals are sporadically found in birds, either in association with clinical signs, such as C. parvum in the stone curlew (Burhinus oedicnemus) (ZYLAN et al., 2008), or asymptomatically in birds, as reported by Qi et al. (2014) for ostriches with Cryptosporidium muris present in their feces.

Epidemiological, Clinical and Pathological Aspects of Cryptosporidium spp. Infection in Birds

Although many recently reported Cryptosporidium infections in the intestinal and respiratory tracts and the bursa of Fabricius in birds are related, respectively, to the presence of C. meleagridis and C. baileyi (RYAN, 2010), the possible roles of other species or genotypes of Cryptosporidium in the etiology of infections that were not characterized molecularly cannot be disregarded. For this reason, in the present review, the denomination Cryptosporidium sp. was used for cases where molecular characterization was not performed, unless the authors defined the species of Cryptosporidium, as in several studies regarding C. baileyi.

There are numerous descriptions of infection by Cryptosporidiumamong several avian species, particularly dating from the 1980s and 1990s, in which the diagnoses were accomplished only through cytological or histopathological observations without molecular characterization of the species or the genotype (GOODWIN, 1989; SRÉTER & VARGA, 2000). The reported clinical signs were mostly related to the respiratory tract and the gastrointestinal tract and were sometimes associated with mortality. However, other tissues have been found to be colonized by Cryptosporidium sp. in clinical or subclinical infections: the bursa of Fabricius, ocular conjunctiva, middle ear, pancreas and kidneys (DHILLON et al., 1981; THAM et al., 1982; HOERR et al., 1986; MASON, 1986; RITTER et al., 1986; O'DONOGHUE et al., 1987; GOODWIN, 1988; NAKAMURA & ABE, 1988; GOODWIN, 1989; GOODWIN & BROWN, 1989; JARDINE & VERWOERD, 1997; MURAKAMI et al., 2002; SRÉTER & VARGA, 2000; RYAN, 2010).

The importance of cryptosporidiosis in commercial poultry production has not yet been determined because few studies on the influence of natural infection by Cryptosporidium spp. on the production parameters of these birds have been conducted. Snyder et al. (1988) investigated antibodies against Cryptosporidiumspp. by means of the indirect ELISA technique among broiler chickens in the United States and observed that the flocks that presented the best performance were negative for Cryptosporidium. However, positive Cryptosporidium serology was not clearly correlated with poor performance. Other authors have reported positive correlations between the presence of C. baileyi infection in broiler chickens and decreased weight gain, greater incidence of airsacculitis, increased mortality and greater carcass condemnation rates in slaughterhouses (GORHAM et al., 1987; GOODWIN et al., 1996).

Infection by Cryptosporidium spp. in several species of wild and domestic birds has been demonstrated by many studies, with the reported prevalence values ranging from 0.8 to 44.4% (Table 2).

Table 2 Worldwide prevalence of Cryptosporidium spp. in wild and domestic birds. 

Host species Geographic origin Species/genotype % positive for Cryptosporidium spp. (No. positive/No. sampled) References
Alectoris rufa Czech Republic C. baileyi, C. meleagridis 22 (145/663) Máca & Pavlásek (2015)
Anas platyrhynchos China C. baileyi 16.6 (92/564) Wang et al. (2010)
Columba livia domestica Iran Cryptosporidiumspp. 2.94 (3/102) Radfar et al. (2012)
China C. baileyi, C. meleagridis 0.8 (2/244) Li et al. (2015)
Coturnix coturnix japonica C. baileyi, C. meleagridis 13.1 (239/1818) Wang et al. (2012)
Gallus gallus domesticus China C. baileyi, C. meleagridis 8.9 (179/2015) Wang et al. (2010)
Algeria C. baileyi, C. meleagridis 34.4 (31/90) Baroudi et al. (2013)
China Avian genotype II, C. baileyi, C. meleagridis 9.87 (38/385) Wang et al. (2014b)
Meleagris gallopavo Iran Cryptosporidiumspp. 35.3 (17/60) Gharagozlou et al. (2006)
USA C. parvum 6.3 (5/79) McEvoy & Giddings (2009)
Algeria C. meleagridis 43.9 (25/57) Baroudi et al. (2013)
Several
species
Australia Avian genotypes I, II, III, C. andersoni, C. baileyi, C. galli, C. muris 6.25 (27/430) Ng et al. (2006)
Brazil Avian genotypes I, II, III, C. baileyi, C. galli, C. meleagridis, C. parvum 4.86 (47/966) Nakamura et al. (2009)
China Avian genotypes I, II, III, V, C. baileyi, C. galli, C. meleagridis, C. parvum 8.1 (35/434) Qi et al. (2011)
Brazil Avian genotype II, C. baileyi, C. galli 6.6 (16/242) Sevá et al. (2011)
Nigeria Cryptosporidiumspp. 7.4 (66/890) Bamaiyi et al. (2013)
Spain C. meleagridis, C. parvum 8.3 (36/433) Reboredo-Fernández et al. (2015)
Struthio camelus Brazil Cryptosporidiumspp. 44.4 (50/77) Oliveira et al. (2008)
China C. baileyi 11.7 (53/452) Wang et al. (2011)
Vietnam Avian genotype II 23.7 (110/464) Nguyen et al. (2013)
China C. baileyi, C. muris 10.2 (31/303) Qi et al. (2014)

Intestinal Infection by Cryptosporidium sp., C. meleagridis and C. parvum

In turkeys, infection by C. meleagridis either presents subclinical characteristics (BERMUDEZ et al., 1988; WOODMANSEE et al., 1988) or has a clinical manifestation in the form of enteritis (SLAVIN, 1955; GOODWIN et al., 1988). In some cases, the infection is associated with other infectious agents (WAGES & FICKEN, 1989). Clinical infection is characterized by decreased weight gain, diarrhea, small intestine distention by gas and mucus, and the presence of evolutionary stages of Cryptosporidium in the proximal and distal portions of the small intestine (GOODWIN et al., 1988; GHARAGOZLOU et al., 2006).

Although C. meleagridis infects domestic chickens (LINDSAY et al., 1989), clinical cryptosporidiosis related to intestinal infection occurs infrequently. Additionally, there are only occasional reports of intestinal cryptosporidiosis in domestic chickens, which is usually subclinical or associated with clinical signs in co-infections with other etiological agents (TYZZER, 1929; ITAKURA et al., 1984; GOODWIN, 1988; GOODWIN & BROWN, 1989).

Infection by Cryptosporidium sp. has been correlated with the occurrence of enteritis and high mortality among quail, with the presence of diarrhea, small intestine containing clear aqueous fluid, cecum containing brown and foamy fluid, atrophy of the intestinal villi and presence of detached enterocytes in the intestinal lumen, as well as epithelial colonization by Cryptosporidium (HOERR et al., 1986). Cryptosporidium sp. in either natural infections (RITTER et al., 1986) or experimental infections (GUY et al., 1987), with or without associations with reoviruses, causes severe intestinal infection and high mortality among quail, in addition to presenting synergism with reoviruses.

One report described C. meleagridis infection in a breeding farm of red-legged partridges (Alectoris rufa) with clinical signs characterized by diarrhea and coughing, morbidity of 60-70% and mortality of 50% (100/200). On the same farm, during a later outbreak, mortality reached 89% (400/450). Evolutionary stages of Cryptosporidium were present in the respiratory tracts and intestines of these birds. Because molecular characterization was only performed on the intestinal content, from which C. meleagridis was identified, the authors of the study suggested that the respiratory infection could have been caused by C. meleagridis, although it was an unusual location, or could have been due to co-infection with C. baileyi (PAGÈS-MANTÉ et al., 2007).

Enteritis due to Cryptosporidium sp. has been reported among pigeons, with clinical signs such as diarrhea, hyperemia and intestinal distension and the presence of evolutionary stages of the parasite in the epithelium of the small intestine (ÖZKUL & AYDIN, 1994).

The importance of the prevalence of intestinal infection among Psittaciformes has not been determined. However, intestinal cryptosporidiosis associated with clinical signs has been observed among budgerigars (Melopsittacus undulatus) (GOODWIN & KRABILL, 1989), cockatiels (Nymphicus hollandicus) (GOODWIN & KRABILL, 1989; LINDSAY et al., 1990), ring-necked parrots (Psittacula krameri) (MORGAN et al., 2000) and lovebirds, which exhibited a high mortality rate (Agapornissp.) (BELTON & POWELL, 1987).

Although infection by C. parvum is not common among birds, Zylan et al. (2008) described a case of catarrhal enteritis and mortality among stone curlews (Burhinus oedicnemus) in Saudi Arabia.

Infection by Cryptosporidium sp., C. baileyiand Avian Genotype II in the Ocular Conjunctiva, Respiratory Tract, Bursa of Fabricius, Rectum and Cloaca

Cryptosporidium sp. and C. baileyi are frequently regarded as etiological agents for infections in the upper respiratory system, middle ear and ocular conjunctiva of wild birds, such as owls (Otus scops), swallows (Petrochelidon pyrrhonota), falcons (Falco cherrug and Falco rusticolus X Falco cherrug) and red grouse (Lagopus lagopus scoticus)(VAN ZEELAND et al., 2008; MOLINA-LÓPEZ et al., 2010; COLDWELL et al., 2012; LEY et al., 2012; BOUGIOUKLIS et al., 2013; BAINES et al., 2014), and of domesticated birds, such as domestic chickens (BLAGBURN et al., 1991), geese (Anser anser f. domestica) (CHVALA et al., 2006), turkeys (GLISSON et al., 1984), ducks (MASON, 1986; O'DONOGHUE et al., 1987), peacocks (MASON & HARTLEY, 1980) and pheasants (RANDALL, 1986).

Respiratory infection may be restricted to the upper respiratory tract, or it may disseminate to the lower respiratory tract, including the bronchia, lungs and air sacs (Figure 1a-c). This may occur with C. baileyi alone or in association with other etiological agents of respiratory infections in chickens, such as Escherichia coli (Figure 1d) and the infectious bronchitis virus, and can result in high mortality (GOODWIN, 1989; BLAGBURN et al., 1987; BLAGBURN et al., 1991; MEIRELES et al., 1999). Several reports have been published on infections by Cryptosporidium sp. in turkeys and quails, with or without associations with other etiological agents (THAM et al., 1982; TARWID et al., 1985; MURAKAMI et al., 2002).

Figure 1 a: Chicken showing dyspnea after intratracheal inoculation of C. baileyi oocysts. b: Light micrograph of chicken trachea. Developmental stages of C. baileyi adhered to the epithelial surface (arrows), epithelial hyperplasia and infiltration of inflammatory cells in the submucosa (H&E stain, 400x). c: Light micrograph of chicken lung tissue. Developmental stages of C. baileyi adhered to the bronchial epithelial surface (arrows), inflammatory cells infiltrating both submucosa and epithelium, and inflammatory exudate filling the bronchial lumen (H&E stain, 200x). d: Scanning electron micrograph of chicken tracheal epithelium showing severe loss of cilia and concomitant infection with C. baileyi (arrow) and Escherichia coli (arrowhead) (2,000x). 

Oral infection by C. baileyi is generally subclinical, although there may be decreased weight gain, which may only be transitory (BLAGBURN et al., 1987; LEVY et al., 1988; MEIRELES et al., 1998a). After oral or intratracheal infection, C. baileyi colonizes the bursa of Fabricius, which presents slight hyperemia and mucus on the mucosal surface. The exudation of products generated from the inflammation, especially heterophils, plasma and cell residues, results in the deposition of a caseous exudate in the lumen of the bursa of Fabricius (Figure 2a) (GUY et al., 1988; MEIRELES et al., 1998b).

Figure 2 a: Caseous exudate filling the lumen of bursa of Fabricius of a chicken infected with C. baileyi. b:Scanning electron micrograph of bursa of Fabricius of a chicken infected with C. baileyi. Massive infection with parasite developmental stages covering the epithelial surface (700x). c:Light micrograph of chicken bursa of Fabricius. Developmental stages of C. baileyi adhered to the epithelial surface, epithelial hyperplasia and inflammatory cells infiltrating both submucosa and epithelium (H&E stain, 400x). d: Light micrograph of ostrich urodeum. Developmental stages of Cryptosporidium avian genotype II adhered to the epithelial surface and inflammatory cell infiltration in the submucosa (H&E stain, 400x). 

Divergent reports exist on the effects of cryptosporidiosis on the immune system. Cryptosporidium baileyi causes a severe infection in the bursa of Fabricius (Figure 2b), which is the organ responsible for the humoral immune response in birds (SCOTT, 2004). Although experimental infections with C. baileyi have been found to present diffuse chronic superficial purulent bursitis with epithelial hyperplasia and hypertrophy (Figure 2c) and slight lymphoid atrophy (GUY et al., 1988; LEVY et al., 1988; GOODWIN & BROWN, 1989; MEIRELES et al., 1998b), no influence on the humoral immune response of chickens has been observed (BLAGBURN et al., 1987; MEIRELES et al., 1998b; ABBASSI et al., 2000). Nevertheless, other reports have shown that C. baileyi infection had a suppressive effect on the humoral immune response of birds to the pathogenic virus or vaccine virus for Marek’s disease (NACIRI et al., 1989), the Gumboro disease vaccine virus (LEVY et al., 1988), reoviruses (GUY et al., 1988), the Newcastle disease vaccine virus (RHEE et al., 1998a; ELADL et al., 2014), the infectious bronchitis vaccine virus (RHEE et al., 1998b), Brucella abortus (RHEE et al., 1998c) and the avian influenza vaccine virus (HAO et al., 2008; ELADL et al., 2014).

In addition to the possible immunosuppression caused by C. baileyi, even if only transitory, the association of C. baileyi with other infectious agents may result in high mortality and decreased weight gain among chickens. Among the agents that may present synergistically with C. baileyi are the virus vaccine (Rispens) for Marek’s disease (ABBASSI et al., 2000), the avian infectious anemia virus (HORNOK et al., 1998), the Gumboro disease virus (LEVY et al., 1988) and reoviruses (GUY et al., 1988). In contrast, Meireles et al. (1995) did not observe any synergism among broiler chickens that were experimentally infected with Toxoplasma gondii and C. baileyi.

There have been reports that infection by Cryptosporidium sp. in ostriches resulted in prolapse of the phallus and cloaca (ALLWRIGHT & WESSELS, 1993; BEZUIDENHOUT et al., 1993; PENRITH & BURGER, 1993; PENRITH et al., 1994) and in pancreatic necrosis (JARDINE & VERWOERD, 1997). The avian genotype II colonizes the epithelium of the cloaca (Figure 2d) and, less frequently, the rectum and bursa of Fabricius of ostriches. The infection results in prolapse of the cloaca (Figure 3a), particularly if stressful conditions lead to immunosuppression or if there are poor husbandry practices relating to feed, water or hygiene (SANTOS et al., 2005).

Figure 3 a: Cloacal prolapse in ostrich chick infected with Cryptosporidium avian genotype II. b:Single oocyst of C. galli (arrow). Fecal sample from a chronically infected adult canary processed using the Sheather's centrifugal flotation procedure (Phase contrast microcopy, 400x). c:Numerous oocysts of Cryptosporidium avian genotype II (arrow). Fecal sample from an ostrich chick processed using the ether centrifugal sedimentation procedure (Malachite green negative stain, 100x). d: Light micrograph of chicken bursa of Fabricius mucosal smear. Developmental stages of C. baileyi (arrow)(Safranin methylene blue stain, 200x).  

Infection in the Proventriculus by Cryptosporidium sp., Cryptosporidium galli, C. muris, Avian Genotype III and the Eurasian Woodcock Genotype

Cryptosporidium galli infects several species of birds of the orders Bucerotiformes, Galliformes, Passeriformes, Phoenicopteriformes and Psittaciformes (Table 1). The pathogenicity of the gastric species of Cryptosporidium has not yet been determined. Gastric infections by C. galli or Cryptosporidiumsp. may be subclinical or associated with clinical signs characterized by apathy, diarrhea, weight loss, and sporadic mortality (BLAGBURN et al., 1990; CLUBB, 1997; MORGAN et al., 2001; ANTUNES et al., 2008; SILVA et al., 2010).

Infection with C. galli is characterized by intermittent and chronic shedding of oocysts in the feces. C. galli is able to infect young and adult birds and cause chronic gastric infection similar to C. serpentis in snakes (SILVA et al., 2010). Thus, Antunes et al. (2008) and Silva et al. (2010)suggested that infections by C. galli could be responsible for chronic proventriculitis in birds, which would predispose them to secondary infections by other pathogens.

The avian genotype III has also been found among several species of Passeriformes and Psittaciformes (Table 2). As with C. galli, avian genotype III causes chronic gastric disease, with clinical signs that include vomiting, weight loss and macroscopic and microscopic lesions in the proventriculus (MAKINO et al., 2010; RAVICH et al., 2014).

Cryptosporidium muris and C. andersoni infect several species of mammals and are occasionally related to clinical signs (SANTÍN, 2013). In birds, C. muris and C. andersoni oocysts may be present in fecal samples, possibly due to an actual infection or to being mechanically transported (NG et al., 2006). Subclinical infection by C. muris, which has apparently adapted to a new host, has been described among adult ostriches in China (QI et al., 2014).

There is only one report of infection in the proventriculus that was caused by the Eurasian woodcock genotype; this infection was described in the Czech Republic in a Eurasian woodcock (Scolopax rusticola) that died during the quarantine period (RYAN et al., 2003b).

Infection by Other Avian Genotypes of Cryptosporidium

Tissue tropism or the clinical importance of other genotypes of Cryptosporidium among birds has not been determined. Avian genotype I and avian genotype V show genetic similarity to C. baileyi and avian genotype II (ABE & MAKINO, 2010; MEIRELES et al., 2006; NG et al., 2006). Because species with greater genetic similarity present similar tissue tropism, as observed with C. parvum and C. meleagridis, with C. baileyi and avian genotype II and with C. galli and avian genotype III (XIAO et al., 2004; NG et al., 2006), it is likely that avian genotype I and avian genotype V colonize the final portion of the intestine, cloaca, bursa of Fabricius or respiratory system, and avian genotype IV, the proventriculus.

The hosts of the other avian genotypes described to date are as follows: avian genotype I: the canary (Serinus canaria) (NG et al., 2006; NAKAMURA et al., 2009) and the Indian peafowl (Pavo cristatus) (NAKAMURA et al., 2009); avian genotype IV: the Japanese white-eye (Zosterops japonicus) (NG et al., 2006); and avian genotype V: the cockatiel (Nymphicus hollandicus) (ABE & MAKINO, 2010; QI et al., 2011) and the blue-fronted parrot (Amazona aestiva) (NAKAMURA et al., 2014).

Diagnosis of Cryptosporidiosis Among Birds

Experience is a fundamental factor in diagnosing cryptosporidiosis because Cryptosporidium oocysts are small in comparison with other coccidians, do not present sporocysts, are difficult to observe, and are morphologically similar to fungi and yeast spores (CASEMORE, 1991). In samples with few oocysts in particular, care is needed to avoid false-positive results in fecal samples examined using the most common diagnostic methods, such as acid-fast staining or viewing oocysts under an optical microscope after concentration with saturated solutions of sugar, zinc sulfate or sodium chloride.

False-negative results are also common in samples with a low number of oocysts because of the low sensitivity of the staining techniques (JEX et al., 2008). In infections with C. galli, chronic shedding occurs, and few oocysts (Figure 3b) are observed per slide (ANTUNES et al., 2008). The amount of oocyst shedding and the patent period of infection with C. baileyi and C. meleagridis vary according to the age and species of the host (SRÉTER & VARGA, 2000).

The diagnostic methods using microscopy that are most used and least expensive involve screening for oocysts after centrifugal flotation in Sheather’s solution, followed by phase contrast microscopy (Figure 3b) or bright-field microscopy (CARDOZO et al., 2008; TEIXEIRA et al., 2011a) and any of the many staining techniques for fecal samples, including negative malachite green staining (Figure 3c) (ELLIOT et al., 1999) and acid-fast staining (HENRIKSEN & POHLENZ, 1981; ORTOLANI, 2000; CARDOZO et al., 2008). In morphometric studies, morphological and morphometric alterations in oocysts should be considered when fecal smears are subjected to staining techniques (MEIRELES & FIGUEIREDO, 1992; CARDOZO et al., 2005).

Several staining techniques are useful for screening of the evolutionary stages of Cryptosporidium in histological sections and in mucosal smears, including hematoxylin and eosin, safranin-methylene blue (Figure 3d) and acid-fast stains (Figure 4). Furthermore, Cryptosporidium DNA can be detected in tissue sections using fluorescent in situ hybridization (LATIMER et al., 1988; CHVALA et al., 2006; JEX et al., 2008).

Figure 4 Light micrograph of lesser seed-finch proventriculus mucosal smear. Developmental stages of C. galli (arrow) (Kinyoun acid-fast stain, 1,000x). 

Immunological methods for Cryptosporidium spp. diagnosis have been extensively reviewed (JEX et al., 2008; CHALMERS & KATZER, 2013). The detection of Cryptosporidium by capture enzyme-linked immunoassays (ELISA) or direct fluorescent antibody (DFA) assays using commercially available antibodies have been extensively adopted in fecal and environmental samples; as a rule, they present higher sensitivity and higher specificity than oocyst-staining techniques.

The antigens targeted by capture ELISA and DFA present cross-reactivity among the different species of Cryptosporidium, and therefore, does not allow species-specific diagnosis (GRACZYK et al., 1996; JEX et al., 2008; CHALMERS et al., 2011; TEIXEIRA et al., 2011b). Although both methods are commonly applied to detect C. parvum antigens (JEX et al., 2008), they may be useful for the diagnosis of avian cryptosporidiosis (RICHTER et al., 1994; GRACZYK et al., 1996; ROHELA et al., 2005; PAGÈS-MANTÉ et al., 2007).

Although the oocysts of some species present distinct morphology and morphometry, microscopic analysis does not allow species characterization because small variations exist in these parameters, and in many cases, the oocysts may be identical between different species or genotypes (RYAN, 2010). However, a presumptive diagnosis of gastric, intestinal or respiratory/bursal/cloacal cryptosporidiosis in birds can be accomplished by the presence of ellipsoidal oocysts measuring 7.5-8.5 × 6.0-6.4 µm; spherical, irregularly spherical or slightly elongated oocysts measuring 4.5-6.0 × 4.2-5.3 µm; or ovoid oocysts measuring 6.0-7.5 × 4.8-5.7 µm, respectively (CURRENT et al., 1986; LINDSAY et al., 1989; RYAN, 2010).

Molecular characterization of Cryptosporidium is performed by means of PCR, followed by either restriction fragment length polymorphism (RFLP) or sequencing of the amplified fragments. The gene most used for determining the species or genotype is 18S rRNA (RYAN et al., 2014). In comparison with the species of Cryptosporidiumfound in mammals, few sequences for the Cryptosporidium of avian species have been published in GenBank. When better resolution is needed to identify genetically similar species or genotypes, the relevant sequences of avian Cryptosporidium that are available relate to actin gene, heat shock protein gene (HSP-70) and Cryptosporidium oocyst wall protein gene (COWP) (Table 1). The 60-kDa glycoprotein (GP60) gene is used for subtyping C. meleagridis in molecular epidemiology studies (STENSVOLD et al., 2014; WANG et al., 2014a).

The genetic similarity between avian genotype II and avian genotype V in the 18S rRNA gene is 99.9%. Only a substitution of G by A in positions 329 and 378 differentiates the sequences of avian genotype II (DQ290031) and avian genotype V (AB471646), respectively. Because of this genetic similarity and the possibility of intraspecies variations in the 18S rRNA gene, classification of these two avian genotypes is recommended only after at least one gene that presents greater interspecies polymorphism, such as the HSP-70 gene or the actin gene (ABE & MAKINO, 2010; NG et al., 2006; MEIRELES et al., 2006), has been analyzed.

Species-specific diagnosis using molecular biology techniques is also possible. Recently, Nakamura et al. (2014) developed a real-time PCR specifically for diagnosing C. galli and avian genotype III.

Treatment and Prophylaxis

Many drugs have been tested for the treatment of cryptosporidiosis, but the US Food and Drug Administration (FDA) has approved only nitazoxanide for use in humans (SMITH & CORCORAN, 2004; STRIEPEN, 2013). Although halofuginone has shown variable efficacy, an effective drug for the prophylaxis and treatment of animal cryptosporidiosis is still lacking (LINDSAY et al., 1987b; SRÉTER et al., 2000; SHAHIDUZZAMAN & DAUGSCHIES, 2012).

Cryptosporidium oocysts are resistant to environmental stress and to the disinfectants commonly used in avian facilities. The prevention and control of avian cryptosporidiosis must rely on rigorous measures related to nutritional and sanitary management to prevent exposure to oocysts and the prophylaxis of concomitant diseases that are commonly associated with avian cryptosporidiosis (SANTOS et al., 2005; SRÉTER & VARGA, 2000; SILVA et al., 2010; SHAHIDUZZAMAN & DAUGSCHIES, 2012).

Importance for Public Health

More than 90% of human Cryptosporidium infections are related to C. hominis or C. parvum, although there are sporadic reports of infections with other Cryptosporidium species or genotypes. Among the Cryptosporidium species and genotypes of avian hosts, only C. meleagridis has a wider host spectrum and is able to infect humans; in fact, it is the third most common cause of human cryptosporidiosis. In some countries, such as Peru and Thailand, C. meleagridis is responsible for 10-20% of human Cryptosporidium infections, with a frequency similar to that of infection by C. parvum (XIAO & FENG, 2008; CHALMERS & GILES, 2010; ELWIN et al., 2012; INSULANDER et al., 2013).

Silverlås et al. (2012) reported the possible zoonotic transmission of C. meleagridis in Sweden when samples with identical nucleotide sequences for the 18S rRNA and HSP-70 genes were found in hens, broiler chickens and an infected person. Further studies using phylogenetic analysis of multiple loci have suggested that the C. meleagridis found in birds may be related to isolates from humans and that birds may constitute an infectious source of human infections by C. meleagridis (STENSVOLD et al., 2014; WANG et al., 2014a).

Epidemiological studies have reported the presence of C. meleagridisin domestic birds and environmental samples. In Algeria, a report showed a high prevalence of C. meleagridis: 34% (26/90) in chickens and 44% (25/57) in turkeys (BAROUDI et al., 2013). However, in China, a low prevalence was described for C. meleagridis among broiler chickens (0.52%; 2/385) (WANG et al., 2014b), laying hens (0.19%; 3/1542) (WANG et al., 2010) and quails (0.22%; 4/1818) (WANG et al., 2012). Li et al. (2012) found C. meleagridis in 24.4% (22/90) of the wastewater samples collected from four cities in China.

The oocysts of C. parvum are sporadically present in fecal samples of asymptomatic birds that are kept either as pets or in zoos. In most situations, the birds represent only a mechanical transporter of oocysts (NAKAMURA et al., 2009; QUAH et al., 2011). However, even if birds are rarely infected by the Cryptosporidium species that are associated with mammals, aquatic birds mechanically transport the oocysts of zoonotic species, such as C. parvum and C. hominis, and may participate in the epidemiological chain of human cryptosporidiosis by means of environmental contamination (GRACZYK et al., 1998; ZHOU et al., 2004; GRACZYK et al., 2008; PLUTZER & TOMOR, 2009).

Concluding Remarks

Among the three species and various genotypes of Cryptosporidiumidentified in birds, only partial information is available regarding their economic, clinical, pathological and epidemiological characteristics and their importance for public health. Most of this information concerns C. baileyi, C. galli, C. meleagridis, avian genotype II and avian genotype III. Birds are kept as pets, for ornamental purposes, in zoos, in wildlife conservation centers and for commercial poultry production. The importance of determining the various aspects of cryptosporidiosis as a zoonosis or as a disease with significance regarding the health of birds is undeniable.

Reports of clinical disease associated with the presence of Cryptosporidium spp. among birds are increasingly frequent. Cryptosporidiosis on commercial farms remains understudied, perhaps because it is a subclinical disease or because it presents clinical signs that are not pathognomonic. Moreover, cryptosporidiosis is not among the diseases that are routinely diagnosed in avian pathology laboratories.

Several aspects of avian cryptosporidiosis, particularly its pathogeny among domestic birds, were more frequently studied during the 1980s and 1990s. After this period, the focus of research on avian cryptosporidiosis was directed toward the detection and classification of species and genotypes of Cryptosporidium and their roles as zoonotic agents. New research related to natural or experimental infection by Cryptosporidium spp. among domestic and wild birds could elucidate factors that are still undefined, such as the importance of this parasite as a primary infection agent and its interaction with other etiological agents of infections in the gastrointestinal tract, respiratory tract and bursa of Fabricius.

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Recebido: 17 de Abril de 2015; Aceito: 24 de Agosto de 2015

*Corresponding author: Marcelo Vasconcelos Meireles. Faculdade de Medicina Veterinária, Universidade Estadual Paulista – UNESP, Rua Clóvis Pestana, 793, Bairro Dona Amélia, CEP 16050-680, Araçatuba, SP, Brasil. e-mail: marcelo@fmva.unesp.br

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