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. 2014 Mar 27:376–393. doi: 10.1533/9780857093912.3.376

Avian diseases which affect egg production and quality

JR Roberts 1, R Souillard 2, J Bertin 3
Editors: Yves Nys, Maureen Bain, Filip Van Immerseel
PMCID: PMC7152417

Abstract

This chapter addresses diseases and syndromes which have been shown, or are reported, to have adverse effects on egg production and quality. However, any disease of poultry can adversely affect egg production and quality indirectly, by affecting the health of the bird. The main topics are the effect on egg production and quality of bacteria (Salmonella, Mycoplasma, Escherichia coli, infectious coryza, Ornithobacterium, Gallibacterium, spirochaetosis), viruses (infectious bronchitis virus, egg drop syndrome, swollen head syndrome, avian encephalomyelitis, influenza, Newcastle disease, laryngotracheitis), syndromes (fatty liver haemorrhagic syndrome, cage layer osteoporosis) and toxic agents. A short section on clinical perspectives reports on information obtained from practising poultry veterinarians as such observations can provide valuable starting points for future research.

Key words: egg quality, avian disease, virus, bacteria

16.1. Introduction

Any disease of poultry can adversely affect egg production and quality either directly, by having effects on the reproductive system, or indirectly, by affecting the health of the bird. Respiratory infections which result in air sacculitis may, in turn, infect the ovary and oviduct. In addition, some diseases infect the oviduct and ovary by ascending infection. It is frequently difficult to diagnose the cause or causes of reduced egg quality because it is often a combination of factors that leads to poor egg quality. Management, nutrition and disease may, in combination, result in a reduction in egg internal quality and/or egg shell quality. The most recent comprehensive review of diseases affecting egg quality is that of Spackman (1987) who, although focusing on egg shell quality, also discussed the effects of disease on egg internal quality. This chapter addresses diseases and syndromes which have been shown, or are reported to, have adverse effects on egg production and quality. Emphasis will be on developments since Spackman’s 1987 review, except where earlier information is fundamental to the discussion. The main experimental developments that have occurred since Spackman’s review are new information about the effect of Australian strains of infectious bronchitis virus on the oviduct and egg quality and the reporting of egg apex abnormalities caused by Mycoplasma synoviae (particularly in combination with infectious bronchitis virus).

16.2. Effects of bacteria on egg production and quality

16.2.1. Salmonella

Aetiology

The genus Salmonella (family Enterobacteriaceae) consists of more than 2500 serologically distinguishable variants and can be divided into non-motile and motile serotypes (Gast, 2008). All salmonellae that are associated with poultry are members of a single genetically defined species, Salmonella enterica.

Epidemiology

The non-motile serotypes, Salmonella enterica serovar Gallinarum (fowl typhoid) and Salmonella enterica serovar Pullorum (pullorum disease), can cause septicaemic disease in poultry. The motile serotypes are often referred to as paratyphoid (PT) salmonellae and include S. enterica serotype Enteriditis and S. enterica serotype Typhimurium (usually abbreviated as S. Enteritidis and S. Typhimurium). The paratyphoid salmonellae are often asymptomatic in avian species, but can cause food-borne illness in humans (Gast, 2008). Age and genetic strain influence the resistance of birds to avian enteric salmonellosis (Beal et al., 2005, Berchieri et al., 2001).

Clinical signs in layers: egg production and quality

In general, young birds are more susceptible to Salmonella infections than mature birds. S. Gallinarum and S. Pullorum cause septicaemic disease resulting in decreased egg production and hatchability, as well as morbidity and mortality (Shivaprasad, 2000). Transovarian infection can occur (Berchieri et al., 2001). Experimental infection of birds with Salmonella Enteritidis increased the incidence of hairline cracks in eggs, leading to an increased risk of contamination (Guard-Bouldin and Buhr, 2006).

16.2.2. Mycoplasma

Aetiology

Mycoplasmas are eubacteria devoid of cell walls and are members of the class Mollicutes, Order I Mycoplasmatales. Genus I, Mycoplasma, has more than 100 species of which 25 infect avian species, and 10 of which infect chickens (Kleven, 2008).

Epidemiology

Mycoplasma gallisepticum causes chronic respiratory disease (CRD) in chickens as well as infectious sinusitis in turkeys and often co-occurs with a respiratory virus infection (Ley, 2008). Oviduct infection can occur owing to proximity to infected air sacs (Nunoya et al., 1997). M. synoviae also causes respiratory disease but can become systemic, causing disease primarily in joints and tendon sheaths in chickens and turkeys (Kleven, 2008). M. gallisepticum and M. synoviae also infect a range of other avian species.

Clinical signs in layers: egg production and quality

Spackman (1987) states ‘The role of Mycoplasmata in egg production and quality is somewhat controversial’. At that time, it was not clear to what extent Mycoplasma synoviae (MS) or M. gallisepticum (MG), alone, were involved in abnormal eggshells and production losses and what was caused by interactions with other infectious agents such as infectious bronchitis virus (Giambrone et al., 1977). MG had been implicated in production losses and, in the case of breeder flocks, decreased hatchability. Until about 2000, the main concern in flocks of laying hens was Mycoplasma gallisepticum ( Kleven, 2008, Kleven et al., 1990; Stipkovits and Kempf, 1996; Yoder 1986) although there were reports of MS in layer flocks (Branton et al., 1989, Mohammed et al., 1986, Mohammed et al., 1987a, Mohammed et al., 1987b, Morrow et al., 1990, Opitz, 1983, Reece et al., 1986a). MS was regarded as being a problem predominantly in broiler and turkey flocks and has also been reported from other poultry species such as ducks (Bencina et al., 1988a, YAMADA and MATSUO, 1983), geese (Bencina et al., 1988b) and pigeons (Reece et al., 1986b). The production of eggs with abnormal shells has been reported for geese infected with Mycoplasma sp strain 1220 (Dobos-Kovacs et al., 2009). The vertical transmission of MS was recognized relatively early (Carnaghan, 1961, Macowan et al., 1984, Roberts and Mcdaniel, 1967). Both MG and MS have the potential to cause salpingitis in laying birds (Domermuth et al., 1967). Opitz (1983) reported MS infection on 48% of farms surveyed in Maine, US. Mohammed et al. (1986) reported prevalence of MG as 73% in southern California and 3% in central California and MS as 91% in southern California and 32% in central California. An economic analysis indicated that there was no association between MS infection and egg production but that MG resulted in an estimated 127 million eggs lost in southern California (Mohammed et al., 1987b).

A recent study by Feberwee et al. (2009a) has shown that MS, isolated from the oviduct of birds producing abnormal eggs, can induce eggshell apex abnormalities (EAA). These abnormalities are characterized by changes in the colour and texture of the shell in the region of the air sac. When this region of the egg shell is observed under the scanning electron microscope, the mammillary layer and the lower part of the palisade layer are missing. These EAAs ceased after an injection of long-acting oxytetracycline but reoccurred 12 days later. The incidence of EEAs was higher in the presence of infectious bronchitis virus. The presence of EAAs was accompanied by shell thinning, increased translucency and reduced shell breaking strength. A later experiment with SPF white layers (Feberwee et al., 2009b) investigated the ability of an MS vaccine to protect against egg shell abnormalities in the presence of an infectious bronchitis challenge. EAAs were produced only in birds that were challenged with M. synoviae, whether or not they had been previously vaccinated for MS. Again, this eggshell abnormality was associated with reduced shell strength. Vaccination reduced the incidence and delayed the appearance of EAAs in eggs from birds challenged with MS but did not completely prevent the occurrence of EAAs.

16.2.3. Escherichia coli

Aetiology

Escherichia is the type genus of the family Enterobacteriaciae and E. coli is the type species of the genus Escherichia. E. coli causes colibacillosis in most avian species, with younger birds being most susceptible (Barnes et al., 2008).

Epidemiology

E. coli is commonly found in the intestines of poultry and is transmitted to eggs primarily by faecal contamination of the shell surface followed by entry into the egg.

Clinical signs in layers: egg production and quality

Escherichia coli affects production and, potentially egg quality, in laying hens by causing colibacillosis associated with salpingitis (Trampel et al., 2007). Other avian species such as ducks may also be affected (Bisgaard, 1995). Many serotypes of E. coli are found in poultry but it is only the avian pathogenic E. coli (APEC) which possess specific virulence factors and are capable of causing salpingitis and peritonitis (Landman and Cornelissen, 2006). Salpingitis may be caused by either a systemic infection or by ascending infection of the oviduct from the cloaca. The study of Ozaki and Murase (2009) reported postmortem findings of fibrinous exudates in the vagina, caseous exudates in the upper oviduct, degenerated ovaries and a thickened and oedematous oviduct mucosa. The stress associated with the onset of lay may act as a precipitating factor in colibacillosis outbreaks ( Zanella et al., 2000). Virulent Mycoplasma synoviae can act as a complicating factor in E. coli peritonitis syndrome (Raviv et al., 2007). However, Vandekerchove et al. (2004) concluded that colibacillosis outbreaks are not necessarily associated with other respiratory pathogens.

16.2.4. Ornithobacterium

Aetiology

Ornithobacterium rhinotracheale is a Gram-negative, non-motile, pleomorphic, rod-shaped, non-sporulating bacterium (Chin et al., 2008).

Epidemiology

O. rhinotracheale causes respiratory disease in chickens and a wide range of other avian species (van Empel and Hafez, 1999). A high seroprevalence of O. rhinotracheale was found in a study in the north central region of the United States (Heeder et al., 2001). The organism is transmitted vertically (van Empel and Hafez, 1999).

Clinical signs in layers: egg production and quality

Clinical signs are respiratory disease and the severity of the disease is worsened when birds have coexisting infections with other respiratory disease agents (Thachil et al., 2009). It can also develop into peritonitis. In commercial laying flocks, O. rhinotracheale results in production drops, decreased egg size, misshapen eggs and increased mortality (Sprenger et al., 2000). Similar symptoms have been reported for flocks of broiler breeders (Chin et al., 2008).

16.2.5. Gallibacterium

Aetiology

The genus Gallibacterium is in the family Pasteurellaceae and contains avian bacteria formerly known as Pasteurella haemolytica, Actinobacillus salpingitidis or Pasteurella anatis. It includes the species G. anatis and G. genomospecies 1 and 2. G. anatis comprises two biovars, a haemolytic biovar haemolytica and a non-haemolytic biovar anatis (Barnes et al., 2008, Christensen et al., 2003, Neubauer et al., 2009).

Epidemiology

Gallibacterium spp can be isolated from a wide variety of birds.

Clinical signs in layers: egg production and quality

Gallibacterium anatis, biovar haemolytica, has been suggested as causing peritonitis and salpingitis in chickens (Christensen et al., 2003; Barnes and Nolan, 2008) and other species (Bisgaard, 1995) and has been isolated from laying birds suffering from reproductive disorders (Neubauer et al., 2009 ). Similar symptoms have been induced experimentally (Bojesen et al., 2004).

16.2.6. Spirochaetosis

Aetiology

Spirochaetes are classified in the Order Spirochaetales which contains three families, Spirochaetaceae, Brachyspiraceae and Leptospiraceae, and a total of nine genera (Hampson and Swayne, 2008). However, spirochaetes which cause avian intestinal spirochaetosis (AIS) are all of the family Brachyspiraceae, genus Brachyspira.

Epidemiology

AIS occurs primarily in flocks of layers and broiler breeder hens so is a disease of birds that are producing eggs. A survey conducted in eastern Australia reported that birds in 43% of broiler breeder and 68% of layer flocks were infected with intestinal spirochaetes but no broiler flocks were infected (Stephens and Hampson, 1999). This study identified Serpulina pilosicoli (now B. pilosicoli) and S. intermedia (now B. intermedia) among the flocks but could not identify other species found. Colonization can be enhanced by a wheat-based diet (Phillips et al., 2004) and this could not be consistently and significantly reduced by the use of endogenous feed enzymes. A recent paper (Ivanics et al., 2009) reported problems in Hungary in layer flocks.

Clinical signs in layers: egg production and quality

Intestinal spirochaetes colonize the caecum and/or rectum and can cause diarrhoea (Hampson and Swayne, 2008, Ivanics et al., 2009). The disease also results in reduced egg production and hatchability and eggshell quality deteriorates (Ivanics et al., 2009).

16.3. Effects of viruses on egg production and quality

16.3.1. Infectious bronchitis virus

Aetiology

Infectious bronchitis (IB) is a poultry viral disease caused by a coronavirus, an enveloped RNA virus. The coronavirus belongs to the Coronaviridae family. The essential coronavirus characteristic is antigenic plasticity, because of the variable amino acid sequences of spicules on the surface. Many serotypes exist and the most frequent is the Massachussetts strain, and new variants like the ‘Qx’ strain.

Epidemiology

IB affects Gallus of all ages, but is more severe in young poultry. The virus spreads in aerosol and is transmitted by the respiratory route. Droppings and nasal discharge are the virulent matter. Transmission is horizontal either directly from bird to bird or indirectly via personnel or material (Cavanagh and Gelb, 2008).

Clinical signs in layers: egg production and quality

With both respiratory and genital tropism, IB infection involves respiratory signs in broilers, drops in egg production and deterioration in egg quality in layers. Some strains are also nephropathogenic. Sevoian and Levine observed internal and external egg quality alteration in laying hens experimentally infected with Massachussetts IB strain (Sevoian and Levine, 1957).

In layers, the disease causes drops in egg production, commonly by from 5 to 10%, and by up to 50%. A commercial chicken flock from which IB virus was recovered showed a drop in egg production of 15%. The drop lasted for approximately 4 weeks and production did not return to the preinfection level (Cook, 1984). The severity of the production drop may vary with the period of lay and with the causative virus strain. An Arkansas strain experimental infection in White Leghorn layers studied the effects of the virus on egg production (Muneer et al., 1986). Infected hens laid fewer eggs and the shell quality and internal quality were inferior. Egg production was 62% in infected birds and 77% in controls 15 days post-infection. IB- infected hens laid eggs with a watery albumen consistency and yolk size was smaller.

Chousalkar and Roberts studied the effect of Australian IB strains on egg production and egg quality. The classic ‘IB egg’, an egg that is wrinkled and corrugated, as described by Dhinakar Raj and Jones (1997), was not observed. Although there was no decline in egg production, there was a deterioration of egg internal quality (albumen) and a loss of egg shell colour (Chousalkar and Roberts, 2009). In addition, egg shape changed, with IB causing eggs to become more elongate. Studies of the histopathology of the oviduct of White Leghorn (Chousalkar et al., 2007a), Hy-Line Gray (Chousalkar et al., 2007b) and Isa Brown hens (Chousalkar et al., 2009a) as well as ultrastructural investigations (Chousalkar and Roberts, 2007a, Chousalkar and Roberts, 2007b, Chousalkar et al., 2009a) confirmed that IB induces pathology in various regions of the oviduct of laying hens. Virus was also isolated from the oviduct of previously challenged laying hens (Chousalkar et al., 2009b).

Coronavirus infection in the shell gland cells causes declines in egg shell quality: thin, soft, misshapen or pale unpigmented shells. The thin and watery albumen occurs when the coronavirus affects the cells of the magnum. Haugh unit values are reduced. A day-old coronavirus infection can also create false layers. Layers are then unable to lay due to the oviduct damage. This situation has been described in France in breeders and layers associated with a new variant strain, Qx (Robineau and Moalic, 2009).

16.3.2. Egg drop syndrome (EDS)

Aetiology

Egg drop syndrome (EDS) virus is caused by duck adenovirus A and was first described in laying hens in 1976. The adenovirus is a member of the genus Atadenovirus and family Adenoviridae.

Epidemiology

Egg drop syndrome affects chickens and quail. Ducks and geese seem to be natural hosts of the virus. The virus is transmitted vertically by eggs. Droppings also contain the virus that can be horizontally transmitted by the oral route. Infected wild birds can be a contamination source for poultry (Adair and Smyth, 2008).

Clinical signs in layers: egg production and quality

The disease is characterized by drops in egg production and increased incidence of abnormal eggs. Birds remain generally healthy. Egg production is usually reduced by from 10% to 40%. The fall in production can be rapid, and the drop in egg production usually lasts from 4 to 10 weeks (McFerran and Smyth, 2000). The first sign is loss of shell pigments. This loss of colour is followed by thin, soft, rough and granular shell and shell-less eggs. Higashihara and coworkers observed few clinical signs except production of abnormal eggs in hens infected orally with EDS virus (Higashihara et al., 1987). Egg production was about 20% lower and aberrant eggs were shell-less, soft-shelled, thin shelled and pale coloured. In this study, internal quality was not altered. In EDS 76 field cases reported by V an Eck, watery and thin albumen was reported (Van Eck et al., 1976).

16.3.3. Swollen head syndrome

Aetiology

Swollen head syndrome is an infectious disease caused by an avian pneumovirus from the Paramyxoviridae family. The virus is enveloped. It is a single-stranded, RNA virus 80-200 nm.

Epidemiology

The swollen head syndrome affects chickens and guinea fowl. Respiratory signs occur in young birds and the adults are affected by drops in egg production. The transmission of the virus is lateral by aerosol through the respiratory route. It is spread by both airborne and mechanical (feed, water and equipment) routes (Gough and Jones, 2008).

Clinical signs in layers: egg production and quality

Respiratory signs occur in young birds and adults are affected by drops in egg production usually by from 5% to 30%. The disease lasts from 2 to 3 weeks. An avian pneumovirus infection study using laying hens was conducted by Cook. Intravenous inoculation caused a drop in egg production of up to 25% and a high incidence of soft and thin-shelled eggs. Some respiratory signs were also observed (Cook et al., 2000).

16.3.4. `Avian encephalomyelitis

Aetiology

Avian encephalomyelitis is a poultry viral disease caused by a picornavirus from the Picornaviridae family. It is an RNA virus, not wrapped and icosahedric.

Epidemiology

Avian encephalomyelitis affects chickens, pheasants, quails and turkeys. The disease occurs in young birds, usually less than three weeks of age and also in layers. Vertically transmission in eggs is the main route of contamination. The virus is also excreted in faeces by the horizontal route from bird to bird (Calnek, 2008).

Clinical signs in layers: egg production and quality

The disease is characterized by neurological signs in young birds with uncoordination, ataxia and tremors. Affected laying hens show a temporary drop in egg production (5-10%), but not neurological signs. Meroz reported a severe drop in egg production of from 75% to 51% associated with encephalomyelitis in a commercial laying flock aged 43 weeks (Meroz et al., 1990). Production returned to its previous level within two weeks. No clinical signs and no abnormal eggs were observed in the flock.

16.3.5. Influenza

Aetiology

Avian influenza is a viral infection caused by influenza A virus, which is a member of the family Orthomyxoviridae. These are RNA viruses classed in three types A, B and C. Influenza A viruses are isolated in birds, swine, horse and human. Types C and D are isolated in humans. The glycoproteins haemagglutinin (H) and neuraminidase (N) characterize the virus subtypes. 16 H antigens and 9 N antigens have been described by Swayne and Halvorson (2008).

Epidemiology

Influenza virus has been recovered from domestic and wild avian species all over the world. Migratory waterfowl are a wild reservoir of influenza virus. Turkeys and chickens are highly susceptible. Avian influenza virus transmission is horizontal and includes direct and indirect contact (Swayne and Halvorson, 2008).

Clinical signs in layers: egg production and quality

Clinical signs vary depending on species infected, bird age and the virulence of the viral subtype. Mortality of up to 90%, without any clinical signs of illness, can be observed in a highly pathogenic influenza outbreak. In a low pathogenic outbreak, some birds may also develop general symptoms with cough, diarrhoea, depression, anorexia and drops in egg production. In the United States, influenza A virus was isolated from commercial laying hens 55 weeks old with up to 69% mortality and severe decrease in egg production. Egg production dropped from as high as 80% to 13% (Johnson and Maxfield, 1976). With low pathogenic influenza A virus, egg drop production is less severe. In 1997 and 1998, in Pennsylvania, H7N2 (nonpathogenic) influenza A virus was diagnosed in commercial leghorn laying hens (Ziegler et al., 1999). Mortality was less than 4% and egg production declined by from 2% to 4%.

16.3.6. Newcastle disease

Aetiology

Newcastle disease is an infectious disease affecting domestic and wild birds and is caused by a paramyxovirus, of the family Paramyxoviridae and genus Rubulavirus. The paramyxoviruses are RNA viruses. They are enveloped with two glycoproteins haemagglutinin-neuraminidase (HN) and glycoproteins F, for virus attachment and fusion.

Epidemiology

Newcastle disease affects all poultry species, but the pathogenicity varies with host. Chickens are highly susceptible, but ducks and geese are less susceptible. The virus spreads through horizontal transmission, in bird secretions (nasal discharge) and droppings. Birds are contaminated by inhalation or ingestion directly from bird to bird or indirectly by mechanical means (personal, material). Vertical transmission is controversial. The virus can survive for several weeks in the environment in contaminated manure or material (Alexander and Senne, 2008).

Clinical signs in layers: egg production and quality

Clinical signs are variable depending on host species and virus strain. Newcastle virus is classed into pathotypes velogenic, mesogenic and lentogenic. The viscerotropic velogenic strains cause high mortality and enteritic lesions. Neurotropic velogenic strains cause also high mortality with respiratory and nervous signs. With mesogenic strains, clinical signs are respiratory and nervous with low mortality level. Lentogenic stains cause respiratory disorders particularly in young birds. In adult birds, egg production is affected by mesogenic strains. Layers are depressed and anorexic. A partial to complete drop in egg production is observed. Egg quality is affected with thin-shelled eggs.

16.3.7. Laryngotracheitis

Aetiology

Laryngotracheitis (LT), also known as infectious laryngotracheitis (ILT), is caused by a member of the family Herpesviridae, subfamily Alphaherpesviridae, genus Iltovirus. It is taxonomically identified as Gallid herpesvirus (Guy and Garcia, 2008).

Epidemiology

Laryngotracheitis is a respiratory disease of chickens that can result in production losses due to mortality, morbidity and decreased egg production (Jordan, 1966, BAGUST et al., 1986, Guy and Garcia, 2008). The chicken is the primary natural host and, although the disease may affect chickens of all ages, it is mostly observed in adult birds. However, the onset of lay can affect the rate of shedding of carrier birds (Hughes et al., 1989).

Clinical signs in layers: egg production and quality

Clinical signs involve primarily the respiratory system with nasal discharge, respiratory depression, mucoid tracheitis, sinusitis, conjunctivitis, gasping and expectoration of blood mucus. Decreased egg production and failure to thrive appear to be secondary to the effects on other body systems. There is no direct evidence for effects of ILT on egg quality.

16.4. Effects of syndromes on egg production and quality

16.4.1. Fatty liver haemorrhagic syndrome (FLHS)

Fatty liver haemorrhagic syndrome (FLHS) is a metabolic disease affecting caged hens in high production. It is characterized by fat infiltration into the liver, haemorrhage and mortality. The disease is associated with a high energy ration and probably induced by mycotoxins, hot weather and dietary lipids. High levels of plasma oestradiol also increase the FLHS risk (Haghighi-Rad and Polin, 1981). Clinical signs are essentially mortality in full production and sudden drops in egg production. The disease can cause up to 5% mortality during the laying cycle (Julian, 2005). The liver is friable, enlarged, yellow, engorged with fat and haemorrhagic. Restricted feeding may prevent the disease. Fatty liver and hepatic steatosis is frequently confused with fatty liver syndrome. Hepatic steatosis is associated with a low protein and high energy level in the ration and causes little mortality and egg production drops (Julian, 2005).

16.4.2. Cage layer osteoporosis

Osteoporosis is a metabolic disorder affecting bone structure and reduction in bone mass. The bones are more fragile and susceptible to fractures. The disease may occur with calcium (Ca) depletion. This may occur because of inadequate dietary Ca, vitamin D3 and phosphorus (P) (Julian, 2005). If Ca is insufficient in the diet, in order to produce eggs, hens withdraw the mineral from cortical bone. Phosphorus deficiency causes osteoporosis, often called cage layer fatigue. Phosphorus is essential to the medullary bone structure. Vitamin D3 deficiency results also in osteoporosis by affecting Ca metabolism. Adequate nutrition helps to reduce this disorder. More exercise results also in better bone quality but may not decrease the fracture incidence. Lines resistant to osteoporosis have been selected (Whitehead and Fleming, 2000).

16.5. Effects of toxic agents on production and egg quality

Various toxic agents and contaminants can produce disease in poultry. Contamination of feed with mycotoxins has the potential to reduce production and egg quality (Garaleviciene et al., 2001, Chowdhury and Smith, 2004, Chowdhury and Smith, 2005, Chowdhury et al., 2005, Pandey and Chauhan, 2007). Chowdhury and coworkers showed that mycotoxins result in increased plasma uric acid concentrations, most likely due to effects on the liver, and also cause immunosuppression. Some of these effects are mediated via a reduction in feed intake of the contaminated feed (Suksupath et al., 1989). Egg production in broiler breeders has been shown to be reduced by a mycotoxin but only at relatively high levels (Brake et al., 2002).

Ingestion of crude oil resulted in lower Haugh units in poultry (Ekweozor et al, 2002). Vanadium has also been shown to reduce albumen quality by reducing the amount of crude ovomucin per millilitre of thick egg albumen (Toussant and Latshaw, 1999). The ovomucin content of the thin albumen was not affected by vanadium supplementation of the diet.

16.6. Clinical perspectives

Opinions were sought from poultry veterinarians via organizations such as the American Association of Avian Pathologists, the World Veterinary Poultry Association and the Australian Veterinary Poultry Association. A number of poultry veterinarians offered an opinion from their own clinical experience. A veterinarian from New Zealand commented on the problems associated with rearing birds to point of lay in cages and then placing them in floor systems (barn, free range). This often results in problems with parasites such as worms and coccidia and producers are not always clearly aware of what treatments are required. This veterinarian also mentioned problems with nutrition that are blamed on disease. He is of the opinion that infectious bronchitis tends to be blamed for shell and albumen quality problems when the cause may be something else (or a combination of other factors).

A veterinarian from the UK, Dr David Burch from Octagon Services Ltd, offered the opinion that egg drops are not so much a syndrome as a production failure. Dr Burch maintains a website on which information about disease and egg drops is provided (Burch, 2010). A veterinarian from Australia offered the following list of diseases and other factors which affect egg production and quality: Mycoplasma gallisepticum, Mycoplasma synoviae, Egg Drop Syndrome-76, avian influenza (high and low pathogenicity), Newcastle disease virus, infectious bronchitis virus, turkey rhinotracheitis, avian herpesvirus and avian encephalomyelitis virus. Rarely, paramyxoviruses and other viruses can cause problems. This veterinarian also stressed the importance of management factors in achieving good egg quality: feed, water, heat, cold, electricity and light.

16.7 References and further reading

  1. Adair B.M., Smyth J.A. Iowa, Blackwell Publishing; Ames: 2008. ‘Egg drop syndrome’, in Saif YM Diseases of Poultry 12th Edition. 266–276. [Google Scholar]
  2. Alexander D.J., Senne D.A. Iowa, Blackwell Publishing; Ames: 2008. ‘Newcastle disease’, in Saif YM Diseases of Poultry 12th Edition. 75–100. [Google Scholar]
  3. Bagust T.J., Calnek B.W., Fahey K.J. Gallid-1 herpesvirus infection in the chicken. 3. Reinvestigation of the pathogenesis of infectious laryngotracheitis in acute and early post-acute respiratory disease. Avian Diseases. 1986;30:179–190. [PubMed] [Google Scholar]
  4. Nolan L.K., Barnes H.J. Other bacterial diseases. In: Saif Y.M., editor. Diseases of Poultry 12th Edition. Blackwell Publishing; Ames, Iowa: 2008. pp. 952–970. [Google Scholar]
  5. Barnes H.J., Nolan L.K., Vaillancourt J.P. Iowa, Blackwell Publishing; Ames: 2008. ‘Colibacillosis’, in Saif YM Diseases of Poultry 12th Edition. 691–737. [Google Scholar]
  6. Beal R.K., Powers C., Wigley P., Barrow P.A., Kaiser P., Smith A.L. A strong antigen- specific T-cell response is associated with age and genetically dependent resistance to avian enteric salmonellosis. Infection and Immunity. 2005;73:7509–7516. doi: 10.1128/IAI.73.11.7509-7516.2005. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Bencina D., Tadina T., Dorrer D. Natural infections of duck with Mycoplasma synoviae and Mycoplasma gallisepticum and mycoplasma egg transmission. Avian Pathology. 1988;17:441–449. doi: 10.1080/03079458808436462. [DOI] [PubMed] [Google Scholar]
  8. Bencina D., Tadina T., Dorrer D. ‘Natural infections of geese with Mycoplasma synoviae and Mycoplasma gallisepticum and egg transmission of the mycoplasmas. Avian Pathology. 1988;17:925–928. doi: 10.1080/03079458808436514. [DOI] [PubMed] [Google Scholar]
  9. Berchieri A.J.R., Murphy C.K., Marston K., Barrow P.A. Observations on the persistence and vertical transmission of Salmonella enterica serovars Pullorum and Gallinarum in chickens; effects of bacterial and host genetic background. Avian Pathology. 2001;30:221–231. doi: 10.1080/03079450120054631. [DOI] [PubMed] [Google Scholar]
  10. Bisgaard M. Salpingitis in web-footed birds: prevalence, aetiology and significance. Avian Pathology. 1995;24:443–452. doi: 10.1080/03079459508419084. [DOI] [PubMed] [Google Scholar]
  11. Blackall P.J., Soriano E.V. Iowa, Blackwell Publishing; Ames: 2008. ‘Infectious coryza and related bacterial infection’, in Saif YM Diseases of Poultry 12th Edition. 789–803. [Google Scholar]
  12. Bojesen A.M., Nielsen O.L., Christensen J.P., Bisgaard M. In vivo studies of Gallibacterium anatis infection in chickens. Avian Pathology. 2004;33:145–152. doi: 10.1080/03079450310001652059. [DOI] [PubMed] [Google Scholar]
  13. Brake J., Hamilton P.B., Kittrell R.S. Effects of the tricothecene mycotoxim diacetoxyscirpenol on egg production of broiler breeders. Poultry Science. 2002;81:1807–1810. doi: 10.1093/ps/81.12.1807. [DOI] [PubMed] [Google Scholar]
  14. Branton S.L., Simmons J.D., Hardin J.M. The effect of biological isolation and a molt-inducing regimen on the recovery of Mycoplasma gallisepticum from commercial leghorn hens. Avian Diseases. 1989;33:574–577. [PubMed] [Google Scholar]
  15. Burch D.G.S. Egg drops - not so much a syndrome, more a production failure. http://www.octagon-services.co.uk/articles/poultry/Egg_Drops.pdf [Accessed 21 March, 2010]
  16. Calnek B.W. Iowa, Blackwell Publishing; Ames: 2008. ‘Avian encephalomyelitis’, in Saif YM Diseases of Poultry 12th Edition. 430–441. [Google Scholar]
  17. Carnaghan R.B.A. Egg transmission of infectious synovitis. Journal of Comparative Pathology. 1961;71 doi: 10.1016/s0368-1742(61)80034-9. 297-285. [DOI] [PubMed] [Google Scholar]
  18. Cavanagh D., GELB J. Iowa, Blackwell Publishing; Ames: 2008. ‘Infectious bronchitis’, in Saif YM Diseases of Poultry 12th Edition. 117–135. [Google Scholar]
  19. Chin R.P., Van Empel P.C.M., Hafez H.M. Iowa, Blackwell Publishing; Ames: 2008. ‘Ornithobacterium rhinotracheale infection’, in Saif YM Diseases of Poultry 12th Edition. 765–774. [Google Scholar]
  20. Chousalkar K.K., Roberts J.R. ‘Ultrastructural study of infectious bronchitis virus infection in infundibulum and magnum of commercial laying hens. Veterinary Microbiology. 2007;122:223–236. doi: 10.1016/j.vetmic.2007.01.021. [DOI] [PubMed] [Google Scholar]
  21. Chousalkar K.K., Roberts J.R. Ultrastructural observations on effects of infectious bronchitis virus in eggshell-forming regions of the oviduct of the commercial laying hen. Poultry Science. 2007;86:1915–1919. doi: 10.1093/ps/86.9.1915. [DOI] [PubMed] [Google Scholar]
  22. Chousalkar K.K., Roberts J.R. Effects of Australian strains of infectious bronchitis virus on internal and external quality of hen eggs. Animal Production Science. 2009;49:162–169. [Google Scholar]
  23. Chousalkar K.K., Roberts J.R., Reece R. Comparative histopathology of two serotypes of infectious bronchitis virus (T and N1/88) in laying hens and cockerels. Poultry Science. 2007;86:50–58. doi: 10.1093/ps/86.1.50. [DOI] [PubMed] [Google Scholar]
  24. Chousalkar K.K., Roberts J.R., Reece R. Histopathology of two serotypes of infectious bronchitis virus in laying hens vaccinated in the rearing phase’. Poultry Science. 2007;86:59–62. doi: 10.1093/ps/86.1.59. [DOI] [PubMed] [Google Scholar]
  25. Chousalkar K.K., Cheetham B.F., Roberts J.R. Effects of infectious bronchitis virus vaccine on the oviduct of hens. Vaccine. 2009;27:1485–1498. doi: 10.1016/j.vaccine.2009.01.012. [DOI] [PubMed] [Google Scholar]
  26. Chousalkar K.K., Cheetham B.F., Roberts J.R. LNA probe-based real-time RT- PCR for the detection of infectious bronchitis virus from the oviduct of unvaccinated and vaccinated laying hens. Journal of Virological Methods. 2009;155:67–71. doi: 10.1016/j.jviromet.2008.09.028. [DOI] [PubMed] [Google Scholar]
  27. Chowdhury S.R., Smith T.K. Effects of feeding blends of grains naturally contaminated with Fusarium mycotoxins on performance and metabolism of laying hens. Poultry Science. 2004;83:1849–1856. doi: 10.1093/ps/83.11.1849. [DOI] [PubMed] [Google Scholar]
  28. Chowdhury S.R., Smith T.K. Effects of feeding grains naturally contaminated with Fusarium mycotoxins on hepatic fractional protein synthesis rates of laying hens and the efficacy of a polymeric glucomannan mycotoxin adsorbent. Poultry Science. 2005;84:1671–1674. doi: 10.1093/ps/84.11.1671. [DOI] [PubMed] [Google Scholar]
  29. Chowdhury S.R., Smith T.K., Boermans H.J., Woodward B. Effects of feed-borne Fusarium mycotoxins on hematology and immunology of laying hens. Poultry Science. 2005;84:1841–1850. doi: 10.1093/ps/84.12.1841. [DOI] [PubMed] [Google Scholar]
  30. Christensen H., Bisgaard M., Bojesen A.M., Mutters R., Olsen J.E. Genetic relationships among avian isolated classified as Pasteurella haemolytica, Actinobacillus salpingitidis of Pasteurella anatis with proposal of Gallibacterium anatis gen. nov., comb, nov and description of additional genomospecles within Gallibacterium gen. nov. International Journal of Systematic and Evolutionary Microbiology. 2003;53:275–287. doi: 10.1099/ijs.0.02330-0. [DOI] [PubMed] [Google Scholar]
  31. Cook J.K.A. The classification of new serotypes of infectious bronchitis virus isolated from poultry flocks in Britain between 1981 and 1983. Avian Pathology. 1984;13:733–741. doi: 10.1080/03079458408418570. [DOI] [PubMed] [Google Scholar]
  32. Cook J.K.A., Chesher J., Orthel F., Woods M.A., Orbell S., Baxendale W., Huggins M.B. Avian pneumovirus infection of laying hens: experimental studies. Avian Pathology. 2000;29:545–556. doi: 10.1080/03079450020016788. [DOI] [PubMed] [Google Scholar]
  33. Dhinakar Raj G., Jones R.C. Infectious bronchitis virus: immunopathogenesis of infection in the chicken. Avian Pathology. 1997;26:677–706. doi: 10.1080/03079459708419246. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Dobos-Kovacs M., Varga Z., Czifra G., Stipkovits L. Salpingitis in geese associated with Mycoplasma sp strain 1220. Avian Pathology. 2009;38:239–243. doi: 10.1080/03079450902912127. [DOI] [PubMed] [Google Scholar]
  35. Domermuth C.H., Gross W.B., Dubose R.T. Mycoplasma salpingitis of chickens and turkeys. Avian Diseases. 1967;11:393–398. [PubMed] [Google Scholar]
  36. Ekweozor I.K.E., Granville A.W., Nkanga E.E., Ogbalu O.K. The effects of crude oil contaminated feeds on the yield and quality of eggs of poultry birds (Gallus domesticus) Journal of Agriculture in the Tropics and Subtropics. 2002;103:89–97. [Google Scholar]
  37. Feberwee A., De Vries T.S., Landman W.J.M. Seroprevalence of Mycoplasma synoviae in Dutch commercial poultry farms. Avian Pathology. 2008;37:629–633. doi: 10.1080/03079450802484987. [DOI] [PubMed] [Google Scholar]
  38. Feberwee A., De Wit J.J., Landman W.J.M. Induction of eggshell apex abnormalities by Mycoplasma synoviae: field and experimental studies. Avian Pathology. 2009;38:77–85. doi: 10.1080/03079450802662772. [DOI] [PubMed] [Google Scholar]
  39. Feberwee A., Morrow C.J., Ghorashi S.A., Noormohammadi A.H., Landman W.J.M. Effect of a live Mycoplasma synoviae vaccine on the production of eggshell apex abnormalities induced by a M. synoviae infection preceded by an infection with infectious bronchitis virus D1466. Avian Pathology. 2009;38:333–340. doi: 10.1080/03079450903183652. [DOI] [PubMed] [Google Scholar]
  40. Fernandez R.P., Colindres H.L., Velasquez E., Soriano V.E., Blackall P.J. Protection conferred by bivalent and trivalent infectious coryza bacterins against prevalent serovars of Avibacterium (Haemophilus) paragallinarum in Mexico. Avian Diseases. 2005;49:585–587. doi: 10.1637/7355-031405R1.1. [DOI] [PubMed] [Google Scholar]
  41. Garaleviciene D., Pettersson H., Augonyte G., El Winger K., Lindberg J.E. Effects of mould and toxin contaminated barley on laying hens performance and health. Archives of Animal Nutrition - Archiv fur Tierernahrung. 2001;55:25–42. doi: 10.1080/17450390109386180. [DOI] [PubMed] [Google Scholar]
  42. Gast R.K. Iowa, Blackwell Publishing; Ames: 2008. ‘Salmonella infections’, in Saif YM Diseases of Poultry 12th Edition. 619–689. [Google Scholar]
  43. Giambrone J.J., Eidson C.S., Kleven S.H. Effect of infectious bursal disease on the response of chickens to Mycoplasma synoviae, Newcastle disease virus, and infectious bronchitis virus. American Journal of Veterinary Research. 1977;38:251–253. [PubMed] [Google Scholar]
  44. Gough R.E., Jones R.C. Iowa, Blackwell Publishing; Ames: 2008. ‘Avian metapneumovirus’, in Saif YM Diseases of Poultry 12th Edition. 100–110. [Google Scholar]
  45. Guard-Bouldin J., Buhr F.U. Evaluation of eggshell quality of hens infected with Salmonella Enteritidis by application of compression. Poultry Science. 2006;85:129–135. doi: 10.1093/ps/85.1.129. [DOI] [PubMed] [Google Scholar]
  46. Guy R.K., Garcia M. Iowa, Blackwell Publishing; Ames: 2008. ‘Laryngotracheitis’, in Saif YM Diseases of Poultry 12th Edition. 137–152. [Google Scholar]
  47. Haghighi-Rad F.., Polin D. The relationship of plasma estradiol and progesterone levels to the fatty liver hemorrhagic syndrome in laying hens. Poultry Science. 1981;60:2278–2283. doi: 10.3382/ps.0602278. [DOI] [PubMed] [Google Scholar]
  48. Hampson D.J., Swayne D.E. Iowa, Blackwell Publishing; Ames: 2008. ‘Avian intestinal spirochaetosis’, in Saif YM Diseases of Poultry 12th Edition. 922–940. [Google Scholar]
  49. Heeder C.J., Lopes V.C., Nagaraja K.V., Shaw D.P., Halvorson D.A. Seroprevalence of Ornithobacterium rhinotracheale infection in commercial laying hens in the north central region of the United States. Avian Diseases. 2001;45:1064–1067. [PubMed] [Google Scholar]
  50. Higashihara M., Hiruma M., Houdatsu T., Takai S., Matumoto M. Experimental infection of laying chickens with egg drop syndrome 1976 virus. Avian Diseases. 1987;31:193–196. [PubMed] [Google Scholar]
  51. Hughes C.S., Gaskell R.M., Jones R.C., Bradbury J.M., Jordan F.T.W. Effects of certain stress factors on the re-excretion of infectious laryngotracheitis virus from latently infected carrier birds. Research in Veterinary Science. 1989;46:274–276. doi: 10.1016/S0034-5288(18)31158-5. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. Ivanics E., Glavists R., Thuma A., Simon B., Kaszanyitzky I., Samu P., Dencso U.K., Dan A. Intestinal spirochaetosis (brachyspirosis) in Hungarian laying hen flocks. Magyar Allatorvosok Lapja. 2009;131:323–330. [Google Scholar]
  53. Johnson D.C., Maxfield B.G. An occurrence of avian influenza virus infection in laying chickens. Avian Diseases. 1976;20:422–424. [PubMed] [Google Scholar]
  54. Jordan F.T.W. A review of the literature on infectious laryngotracheitis (ILT) Avian Diseases. 1966;10:1–26. [Google Scholar]
  55. Julian R.J. Production and growth related disorders and other metabolic diseases of poultry - a review. Veterinary Journal. 2005;169:350–369. doi: 10.1016/j.tvjl.2004.04.015. [DOI] [PubMed] [Google Scholar]
  56. Kleven S.H. Iowa, Blackwell Publishing; Ames: 2008. ‘Mycoplasma synoviae infection’, in Saif YM Diseases of Poultry 12th Edition. 845–856. [Google Scholar]
  57. Kleven S.H., Khan M.I., Yamamoto R. Fingerprinting of Mycoplasma gallisepticum strains isolated from multiple-age layers vaccinated with live F strain. Avian Diseases. 1990;34:984–990. [PubMed] [Google Scholar]
  58. Landman W.J.M., Cornelissen R.A. Escherichia coli salpingitis and peritonitis in layer chickens: an overview. Tijdschrift Voor Diergeneeskunde. 2006;131:814–822. [PubMed] [Google Scholar]
  59. Landman W.J.M., Feberwee A. ‘Field studies on the association between amyloid arthropathy and Mycoplasma synoviae infection, and experimental reproduction of the condition in brown layer’s. Avian Pathology. 2001;30:629–639. doi: 10.1080/03079450120092125. [DOI] [PubMed] [Google Scholar]
  60. Landman W.J.M., Feberwee A. Aerosol-induced Mycoplasma synoviae arthritis: the synergistic effect of infectious bronchitis virus infection. Avian Pathology. 2004;33:591–598. doi: 10.1080/03079450400013170. [DOI] [PubMed] [Google Scholar]
  61. Ley D.H. Iowa, Blackwell Publishing; Ames: 2008. ‘Mycoplasma gallisepticum infection’, in Saif YM Diseases of Poultry 12th Edition. 807–834. [Google Scholar]
  62. Macowan K.J., Atkinson M.J., Bell M.A., Bfianch T.F., Randall C.J. Egg transmission of a respiratory isolate of Mycoplasma synoviae and infection of the chicken embryo. Avian Pathology. 1984;13:51–58. doi: 10.1080/03079458408418507. [DOI] [PubMed] [Google Scholar]
  63. Mcferran J.B., Smyth J.A. Avian adenoviroses. Oie Revue Scientifique et Technique. 2000;19:589–601. [PubMed] [Google Scholar]
  64. Meroz M., Elkin N., Hadash D., Abrams M. Egg drop associated with avian encephalomyelitis virus. Veterinary Record. 1990;127:532. (letter) [PubMed] [Google Scholar]
  65. Morrow C.J., Bell I.G., Walker S.B., Markham P.F., Thorp B.H., Whithear K.G. Isolation of Mycoplasma synoviae from infectious synovitis of chickens. Australian Veterinary Journal. 1990;66:121–124. [PubMed] [Google Scholar]
  66. Mohammed H.O., Carpenter T.E., Yamamoto R., Mcmartin D.A. Prevalence of Mycoplasma gallisepticum and M. synoviae in commercial layers in Southern and Central California. Avian Diseases. 1986;30:519–526. [PubMed] [Google Scholar]
  67. Mohammed H.O., Carpenter T.E., Yamamoto R. Evaluation of factors associated with infection of commercial layers with Mycoplasma gallisepticum and M. synoviae. Avian Diseases. 1987;31:470–476. [PubMed] [Google Scholar]
  68. Mohammed H.O., Carpenter T.E., Yamamoto R. Economic impact of Mycoplasma gallisepticum and M. synoviae in commercial layer flocks. Avian Diseases. 1987;31:474–482. [PubMed] [Google Scholar]
  69. Muneer M.A., Halvorson D.A., Sivandan V., Newman J.A., Coon C.N. Effects of infectious bronchitis virus (Arkansas strain) on laying chickens. Avian Diseases. 1986;30:644–647. [PubMed] [Google Scholar]
  70. Neubauer C., De Souza-Pilz M., Bojesen A.M., Bisgaard M., Hess M. Tissue distribution of haemolytica Gallibacterium anatis isolates in laying birds with reproductive disorders. Avian Pathology. 2009;38:1–7. doi: 10.1080/03079450802577848. [DOI] [PubMed] [Google Scholar]
  71. Nunoya T., Kanai K., Yagihashi T., Hoshi S., Shibuya K., Tajima M. Natural case of salpingitis apparently caused by Mycoplasma gallisepticum in chickens. Avian Pathology. 1997;26:391–398. doi: 10.1080/03079459708419221. [DOI] [PubMed] [Google Scholar]
  72. Opitz H.M. Mycoplasma synoviae infection in Maine’s egg farms. Avian Diseases. 1983;27:324–326. [Google Scholar]
  73. Ozaki H., Murase T. Multiple routes of entry for Escherichia coli causing colibacillosis in commercial layer chickens. Journal of Veterinary Medical Science. 2009;71:1685–1689. doi: 10.1292/jvms.001685. [DOI] [PubMed] [Google Scholar]
  74. Pandey I., Chauhan S.S. Studies on production performance and toxin residues in tissues and eggs of layer chickens fed on diets with various concentrations of aflatoxin AFB1. British Poultry Science. 2007;48:713–723. doi: 10.1080/00071660701713534. [DOI] [PubMed] [Google Scholar]
  75. Phillips N.D., La T., Pluske J.R., Hampson D.J. A wheat-based diet enhances colonization with the intestinal spirochaete Brachyspira intermedia in experimentally infected laying hens. Avian Pathology. 2004;33:451–457. doi: 10.1080/0307945042000260620. [DOI] [PubMed] [Google Scholar]
  76. Pingel H., Jeroch H. Proceedings of the VII European Symposium on the Quality of Eggs and Egg Products; Poznan, Poland: 1997. Egg quality as influenced by genetic, management and nutritional factors. 13–27. [Google Scholar]
  77. Raviv Z., Eerguson-Noel N., Laibinis V., Wooten R., Kleven S.H. Role of Mycoplasma synoviae in commercial layer Escherichis coli peritonitis syndrome. Avian Diseases. 2007;51:685–690. doi: 10.1637/0005-2086(2007)51[685:ROMSIC]2.0.CO;2. [DOI] [PubMed] [Google Scholar]
  78. Reece R.L., Beddome V.D., Barr D.A. Diseases diagnosed in replacement layer and breeder chicken flocks in Victoria, Australia, 1977-1985. Veterinary Record. 1986;8:471–475. doi: 10.1136/vr.119.19.471. [DOI] [PubMed] [Google Scholar]
  79. Reece R.L., Ireland L., Scott P.C. Mycoplasmosis in racing pigeons. Australian Veterinary Journal. 1986;63:166–167. doi: 10.1111/j.1751-0813.1986.tb02962.x. [DOI] [PubMed] [Google Scholar]
  80. Roberts D.H., Mcdaniel J.W. Mechanism of egg transmission of Mycoplasma gallisepticum. Journal of Comparative Pathology. 1967;77:439–442. doi: 10.1016/0021-9975(67)90030-8. [DOI] [PubMed] [Google Scholar]
  81. Robineau B., Moalic P.Y. A clinical aspect of infectious bronchitis: the false layers, changes in the coronaviruses involved in France. A clinical aspect of infectious bronchitis: the false layers, changes in the coronaviruses involved in France. 2009;162:155–160. http://www.academie-veterinaire-defrance.org/bulletin/pdf/2009/numero02/155.pdf Bull. Acad. Vet. France. Available from: [Accessed March 19 2008] [Google Scholar]
  82. Sevoian M., Levine P.P. Effects of infectious bronchitis on the reproductive tracts, egg production, and egg quality of laying chickens. Avian Diseases. 1957;1:136–164. [Google Scholar]
  83. Shivaprasad H.L. Fowl typhoid and pullorum disease. Revue Scientifique et Technique de L’Office International Des Epizooties. 2000;19:405–424. doi: 10.20506/rst.19.2.1222. [DOI] [PubMed] [Google Scholar]
  84. Shivaprasad H.L. Iowa, Blackwell Publishing; Ames: 2008. ‘Arizonosis’, in Saif YM Diseases of Poultry 12th Edition. 665–674. [Google Scholar]
  85. Shivaprasad H.L., Barrow P.A. Iowa, Blackwell Publishing; Ames: 2008. ‘Pullorum disease and fowl typhoid’, in Saif YM Diseases of Poultry 12th Edition. 620–636. [Google Scholar]
  86. Spackman D. Egg quality - current problems and recent advances; London, Butterworth: 1987. ‘The effect of disease on egg quality’, in Wells RG and Belyavin CG. 255–282. [Google Scholar]
  87. Sprenger S.J., Halvorson D.A., Nagaraja K.V., Spasojevic R.S., Dutton R.S., Shaw D.P. Ornithobacterium rhinotracheale infection in commercial laying-type chickens. Avian Diseases. 2000;44:725–729. [PubMed] [Google Scholar]
  88. Stephens C.P., Hampson D.J. Prevalence and disease association of intestinal spirochaetes in chicken in Eastern Australia. Avian Pathology. 1999;28:447–454. doi: 10.1080/03079459994461. [DOI] [PubMed] [Google Scholar]
  89. Stipkovics L., Kempf I. Mycoplasmoses in poultry. Revue Scientifique et Technique de L’Office International Des Epizooties. 1996;15:1495–1525. doi: 10.20506/rst.15.4.986. [DOI] [PubMed] [Google Scholar]
  90. Suksupath S., Cole E.A., Cole R.J., Bryden W.L. Proceedings of the Australian Poultry Science Symposium; Sydney: 1989. Toxicity of cyclopiazonic acid in the laying hen. 94. [Google Scholar]
  91. Swayne D.E., Halvorson D.A. Iowa, Blackwell Publishing; Ames: 2008. ‘Influenza’, in Saif YM Diseases of Poultry 12th Edition. 153–184. [Google Scholar]
  92. Thachil A.J., Velayudhan B.T., Shaw D.P., Halvorson D.A., Nagaraja K.V. Pathogenesis of Ornithobacterium rhinotracheale in egg-laying hens with coexisting infectious bronchitis virus and Escherichia coli infections. Journal of Applied Poultry Research. 2009;18:780–788. [Google Scholar]
  93. Toussant M.J., Latshaw J.D. Ovomucin content and composition in chicken eggs with different interior quality. Journal of the Science of Food and Agriculture. 1999;79:1666–1670. [Google Scholar]
  94. Trampel D.W., Wannemuehler, Nolan L.K. Characterization of Escherichia coli isolates from peritonitis lesions in commercial laying hens. Avian Diseases. 2007;51:840–844. doi: 10.1637/7797-111906-REGR1.1. [DOI] [PubMed] [Google Scholar]
  95. Van Eck J.H.H., Davelaar F.G., Van Den Heuvel-Plesman T.A.M., Van Kol N., Kouwenhoven B., Guldie F.H.M. Dropped egg production, soft shelled and shell-less eggs associated with appearance of precipitins to adenovirus in flocks of laying fowl. Avian Pathology. 1976;5:261–272. doi: 10.1080/03079457608418195. [DOI] [PubMed] [Google Scholar]
  96. Van Empel P.C.M., Hafez H.M. Ornithobacterium rhinotracheale: a review. Avian Pathology. 1999;28:217–227. doi: 10.1080/03079459994704. [DOI] [PubMed] [Google Scholar]
  97. Vandekerchove D., De Herdt P., Laevens H., Butaye P., Meulemans G., Pasmans F. Significance of interactions between Escherichia coli and respiratory pathogens in layer hen flocks suffering from colibacillosis-associated mortality. Avian Pathology. 2004;33:298–302. doi: 10.1080/030794504200020399. [DOI] [PubMed] [Google Scholar]
  98. Whitehead C.C., Fleming R.H. Osteoporosis in cage layers. Poultry Science. 2000;79:1033–1041. doi: 10.1093/ps/79.7.1033. [DOI] [PubMed] [Google Scholar]
  99. Yamada S., Matsuo K. Experimental infection of ducks with Mycoplasma synoviae. Avian Diseases. 1983;27:762–765. [PubMed] [Google Scholar]
  100. Yoder H.W. A historical account of the diagnosis and characterization of strains of Mycoplasma gallisepticum of low virulence. Avian Diseases. 1986;30:510–518. [PubMed] [Google Scholar]
  101. Zanella A., Alborali G.L., Bardotti M., Candotti P., Guadagnini P.F., Martino P.A., Stonfer M. Severe Escherichia coli O111 septicaemia and polyserositis in hens at the start of lay. Avian Pathology. 2000;29:311–317. doi: 10.1080/03079450050118430. [DOI] [PubMed] [Google Scholar]
  102. Ziegler A.F., Davison S., Acland H., Eckroade R.J. Characteristics of H7N2 (nonpathogenic) Avian influenza virus infections in commercial layers, in Pennsylvania, 1997-98. Avian Diseases. 1999;43:142–149. [PubMed] [Google Scholar]

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