turkey coronavirus infections
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IdentityTop of page
Preferred Scientific Name
- turkey coronavirus infections
International Common Names
- English: coronaviral enteritis of turkeys; coronaviral enteritis of turkeys, bluecomb disease; coronaviral enteritis of turkeys, bluecomb disease, ce; infectious enteritis of turkeys; transmissible enteritis of turkeys; turkey coronaviral enteritis
Local Common Names
- India: avian monocytosis
- USA: bluecomb disease; mud fever
OverviewTop of page
Turkey coronaviral enteritis, reviewed by Guy (2008a), is an acute, highly contagious enteric disease of turkeys, characterised by depression, anorexia, diarrhoea, and decreased weight gain. It is caused by a coronavirus that is genetically (Breslin et al., 1999; Stephensen et al., 1999; Guy, 2000; Cavanagh et al., 2001) and antigenically (Guy et al., 1997, 2002; Loa et al., 2000) very similar to infectious bronchitis virus (IBV) of the domestic fowl, reviewed by Cavanagh et al. (2005). The severity of the viral disease is exacerbated by enteropathogenic Escherichia coli (EPEC; Guy et al., 2000; Pakpinyo et al., 2002, 2003) and by coincident infection with other viruses e.g. avian astrovirus (Koci et al., 2000; Spackman et al., 2005).
TCoV affects turkeys of all ages but mortality is greatest amongst poults. When it is particularly severe in poults - high mortality, severe growth depression and immunosuppression - during co-infections with EPEC, it may be referred to as poult enteritis and mortality syndrome. A particular manifestation of PEMS is known as spiking mortality of turkeys (SMT), when there is very sudden and high mortality in poults of up to one month of age (Guy, 2008a). It has also been associated with disease in quail in Italy (Circella et al., 2007).
Although TCoV is antigenically related to IBV, vaccines against IBV are not effective against TCoV, because of extensive differences between the protection-inducing spike protein of the two viruses.
Hosts/Species AffectedTop of page
It had long been considered that TCoV infected only turkeys and it is possible that it will only cause disease in turkeys. However, domestic fowl chicks can be infected experimentally with TCoV, the virus growing in the same tissues as in turkeys but without causing clinical disease (Guy et al., 1999; Ismail et al., 2003). TCoV has also been detected in respiratory tissues of experimentally infected chicks (Gomes et al., 2010).
There are a large number of coronaviruses amongst avian species, broadly resembling IBV in genome organization and gene sequence but with different host ranges and tissue tropisms (Hughes et al., 2009; Muradrasoli et al., 2010; Chu et al., 2011).
Ismail et al. (2001) showed that a classical BCoV isolate, DB2, can cause enteritis in poults.
DistributionTop of page
The disease was initially described in North America where it had great economic impact particularly in the 1950s to the mid-1970s. It has been detected in most turkey producing regions of the USA (Lin et al., 2002; Jindal et al., 2010) and in Canada (Gomaa et al., 2008). TCoV was not detected elsewhere until 2001 in the UK (Cavanagh et al., 2001), although the virus might well have been present earlier. It has subsequently been described elsewhere in Europe (Circella et al., 2007; Maurel et al., 2011) and in Brazil (Teixeira et al. 2007; Bunger et al., 2009).
Distribution TableTop of page
The distribution in this summary table is based on all the information available. When several references are cited, they may give conflicting information on the status. Further details may be available for individual references in the Distribution Table Details section which can be selected by going to Generate Report.
|Continent/Country/Region||Distribution||Last Reported||Origin||First Reported||Invasive||Reference||Notes|
|USA||Present||Present based on regional distribution.|
|-Georgia||Widespread||Goodwin et al., 1995; Guy, 1998|
|-Indiana||Widespread||Guy et al., 1997|
|-Minnesota||Widespread||Adams and Hofstad, 1972a; Adams and Hofstad, 1972b; Sieburth and Johnson, 1957; Dees et al., 1972; Panigrahy et al., 1973; Gonder et al., 1976; Patel et al., 1977|
|-North Carolina||Widespread||Guy et al., 1997|
|-Texas||Present||Linares et al., 1999|
|-Virginia||Present||Sieburth and Johnson, 1957|
|-Washington||Present||Peterson and Hymas, 1951|
|UK||Present||Cavanagh et al., 2001|
PathologyTop of page
Coronaviral enteritis (CE)
Postmortem investigation reveals swollen, pale, flaccid duodenum, with intraluminal mononuclear cell exudates.
The target cells for the virus are those of the epithelia of the intestinal tract, the severity of the lesions being most prominent in jejunum, less marked in ileum and caecum (Adams et al., 1970; Deshmukh et al., 1976), and bursa of Fabricius. The villi of the intestines shorten and are then lost. The cytoplasm of the epithelial cells has a granular appearance with nuclear margination of chromatin, and accentuation of the nucleolus. Adams et al. (1970) described an overall decrease in goblet cells, a decrease in microvillus length and separation of epithelium from the lamina propria and decreased enterchromaffin cells. Recovery of the epithelium can be seen to have commenced by 5 days after infection. Although no histopathological changes were described for the bursa of Fabricius, particles resembling coronavirus have been observed in that organ (Ritchie et al., 1973), TCoV antigen demonstrated by immunofluorescence (Patel et al., 1977) and TCoV isolated (Naqi et al., 1972).
DiagnosisTop of page
While suggestive of coronaviral enteritis (CE) or poult enteritis and mortality syndrome (PEMS), the common clinical signs are not diagnostic.
Starving poults exhibit clinical signs similar to those of CE-affected birds but not the histopathological changes in the intestines described in the Pathology section (Deshmukh et al., 1976).
It is most important not to confuse inanition (starve-outs) or water deprivation with CE in birds. Other pathogens can produce similar clinical signs, for example, reovirus (Simmons et al., 1972; Gershowitz and Wooley ,1973; Adams and Hofstad, 1972a), rotavirus and astrovirus infections (see references in Yu et al., 2000), a vibrio bacterial infection (Adams and Hofstad, 1972a) and protozoal infections (Nagaraja and Pomeroy, 1997).
Stunting syndrome of turkeys is similar to CE but does not appear to be associated with TCoVs or IBV. Electronmicroscopy reveals enveloped virus particles which resemble toroviruses, although the turkey viruses were not related antigenically to the mammalian bovine Breda-1 torovirus or bovine Breda-2 virus (Ali and Reynolds, 1998; 2000).
Electronmicroscopy can be used to look for coronavirus particles in gut contents, although care must be taken not to wrongly identify non-coronaviral fringed membranous particles which may be present in preparations of sick and healthy birds (Goodwin et al., 1995).
Indirect immunofluorescence (IIF) and indirect immunoperoxidase (IIP) procedures, performed with antibody from convalescent turkeys can be used to demonstrate the presence of TCoV in sections of intestines from field cases, antigen being detected in epithelial cells of jejunum, ileum, duodenum and caecum. Infected cells can be detected for many weeks after initial infection (Patel et al., 1975; Cardoso et al., 2008). In the USA sera from field turkeys are tested for antibodies to TCoV using either bursal cells or gut sections from experimentally infected poults or turkey embryos, respectively.
The preferred method for isolation of TCoV is the inoculation of turkey embryos or SPF domestic fowl embryos by the amniotic route (Guy et al., 1997; Reynolds, 1998; Guy, 2008b). The embryos should be inoculated with filtered intestinal contents and/or bursal tissue of turkeys suspected of CE (or PEMS). Intestines of the embryos are a source of the virus. For immunofluorescent antibody analysis embryonic tissue should be removed 24-48 hours after inoculation, snap-frozen, sectioned and stored at –70°C. Virus neutralization tests may also be performed to test for TCoV antibodies, using virus grown in turkey embryos.
As TCoV is antigenically related to IBV (Guy et al., 1997, 2002; Loa et al., 2000), serology-based tests for IBV have been used successfully to diagnose infection by TCoV (Weisman et al., 1987; Loa et al., 2000; Gomaa et al., 2009b), including IBV-Beaudette-infected Vero cells as a substrate for the detection by immunofluorescence of turkey antibodies to TCoV (F.A. Culver, P. Britton and D. Cavanagh, unpublished observations).
Similarly, as TCoV is genetically very similar to IBV, reverse transcriptase polymerase chain reaction- (RT-PCR) based tests for IBV have been successfully used or modified to detect TCoV (Breslin et al., 1999a,1999b; Cavanagh et al., 2001; Sellers et al., 2004; Spackman et al., 2005; Culver et al., 2008; Chen et al., 2010).
Immunology of the disease
Immunoglobulin IgA reactive with TCoV was detected in bile and intestinal secretions for at least six months after experimental infection (Nagaraja and Pomeroy, 1978). Local synthesis of antibody might be responsible for the life-long immunity exhibited by convalescent turkeys (Nagaraja and Pomeroy, 1980). Poults inoculated orally with TCoV at two days of age were protected against challenge 20 days later (Gomaa et al., 2009b).
List of Symptoms/SignsTop of page
|Digestive Signs / Abnormal colour of stool in birds, white, green, yellow faeces||Poultry:All Stages||Sign|
|Digestive Signs / Anorexia, loss or decreased appetite, not nursing, off feed||Poultry:All Stages||Sign|
|Digestive Signs / Diarrhoea||Sign|
|Digestive Signs / Mucous, mucoid stools, faeces||Sign|
|General Signs / Dehydration||Poultry:All Stages||Sign|
|General Signs / Generalized weakness, paresis, paralysis||Poultry:All Stages||Sign|
|General Signs / Hypothermia, low temperature||Poultry:All Stages||Sign|
|General Signs / Increased mortality in flocks of birds||Poultry:All Stages||Sign|
|General Signs / Lack of growth or weight gain, retarded, stunted growth||Poultry:All Stages||Sign|
|General Signs / Neck weakness, paresis, paralysis, limp, ventroflexion||Poultry:All Stages||Sign|
|General Signs / Reluctant to move, refusal to move||Poultry:All Stages||Sign|
|General Signs / Sudden death, found dead||Poultry:All Stages||Sign|
|General Signs / Underweight, poor condition, thin, emaciated, unthriftiness, ill thrift||Sign|
|General Signs / Weakness, paresis, paralysis, drooping, of the wings||Poultry:All Stages||Sign|
|General Signs / Weight loss||Poultry:All Stages||Sign|
|Nervous Signs / Dullness, depression, lethargy, depressed, lethargic, listless||Poultry:All Stages||Sign|
|Nervous Signs / Head tilt||Poultry:All Stages||Sign|
|Skin / Integumentary Signs / Soiling of the feathers, vent feathers||Poultry:All Stages||Sign|
|Skin / Integumentary Signs / Soiling of the vent in birds||Poultry:All Stages||Sign|
Disease CourseTop of page
Turkey coronavirus (TCoV) is highly infectious, hence morbidity is about 100%. In coronavirus enteritis (CE) and poult enteritis and mortality syndrome (PEMS) the virus has been detected only in epithelium of the intestinal tract (enterocytes lining the upper portion of intestinal villi) and bursa of Fabricius (follicular and interfollicular epithelium). In CE, birds huddle together for warmth, stop eating, lose weight and have wet droppings. Older birds are depressed, their head and skin darkens. Wings may be seen to droop, back arch and head retract (Nagaraja and Pomeroy, 1997). The incubation period is two to three days but can be slightly more or less (Patel et al., 1977; Nagaraja and Pomeroy, 1997). Clinical signs can be observed for up to two weeks and recovery of weight, if achieved, may take several weeks. Laying birds experience a drop in production. Mortality varies from less than 10% to 50% or more, depending on the age of the birds (higher mortality in younger birds) and their treatment. Infection of gnotobiotic poults with TCoV alone produced only mild disease (Adams and Hofstad, 1972) but addition of gut flora was reported to exacerbate the disease (Larsen, 1979).
EpidemiologyTop of page
The incubation period of turkey coronavirus (TCoV) is two to three days but can be slightly more or less (Patel et al., 1977; Nagaraja and Pomeroy, 1997). The virus has been detected in gut tissues 160 days after experimental infection (Patel et al., 1977) and may be excreted in droppings for several months after the onset of disease, transmission probably being by the faecal-oral route. The virus is probably spread by such agents as people, their vehicles and non-specifically by vermin, and by insects (Calibeo-Hayes et al., 2003).
Impact: EconomicTop of page
Turkey coronaviral enteritis is a major source of economic loss in the turkey industry, both in poults and older birds (Gomaa et al., 2009a). There is no vaccine.
Zoonoses and Food SafetyTop of page
There is no known zoonotic or food safety issue regarding coronavirus enteritis (CE).
Disease TreatmentTop of page
Nagaraja and Pomeroy (1997) have listed a number of treatments that might ameliorate the effects of coronaviral enteritis (CE): additional heat; calf milk replacer (2.5 kg/100 litres, or 25 lb/100 gallon, of drinking water); potassium chloride (100 g/ 100 litres , 450 g/100 gallon, drinking water) added to milk suspension; antibiotics in drinking water, to combat secondary bacterial infections; copper sulfate in the water, to combat secondary intestinal mycosis that might follow antibiotic application; medicated drinking water should be applied for 4-5 days, untreated water for one day, then medicated water for a further 4-5 days.
Prevention and ControlTop of page
Immunization and vaccines
There are no licensed vaccines for coronaviral enteritis (CE). Birds that recover are immune for life.
Birds that recover from CE are carriers of turkey coronavirus (TCoV) for life and shed the virus for months. Therefore farms should be depopulated after CE. Faeces are a source of prolonged contamination of the environment. Beetles and flies may spread the disease. Access to farms should be strictly limited and controlled as part of a general disease security regime. Marketing of turkeys should take into account the prevalence of CE.
ReferencesTop of page
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Distribution MapsTop of page
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