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Riemerella anatipestifer infection

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Riemerella anatipestifer infection

Summary

  • Last modified
  • 03 January 2018
  • Datasheet Type(s)
  • Animal Disease
  • Preferred Scientific Name
  • Riemerella anatipestifer infection
  • Overview

  • Riemerella anatipestifer infection is a septicaemic (acute, peracute, sometimes chronic) disease of primarily ducks and geese, but it also affects turkeys, chickens, pheasants, guinea fowls, quails and sw...

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Pictures

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PictureTitleCaptionCopyright
Histologic section of duck brain (original x50 H&E stain): Riemerella anatiperstifer causing meningitis and vasculitis in a young duck. Note inflammatory response in vessel wall.
TitleHistopathology
CaptionHistologic section of duck brain (original x50 H&E stain): Riemerella anatiperstifer causing meningitis and vasculitis in a young duck. Note inflammatory response in vessel wall.
CopyrightRichard J. Julian
Histologic section of duck brain (original x50 H&E stain): Riemerella anatiperstifer causing meningitis and vasculitis in a young duck. Note inflammatory response in vessel wall.
HistopathologyHistologic section of duck brain (original x50 H&E stain): Riemerella anatiperstifer causing meningitis and vasculitis in a young duck. Note inflammatory response in vessel wall.Richard J. Julian
Fibrinous airsacculitis
TitleGross lesions
CaptionFibrinous airsacculitis
CopyrightTirath Sandhu
Fibrinous airsacculitis
Gross lesionsFibrinous airsacculitisTirath Sandhu

Identity

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Preferred Scientific Name

  • Riemerella anatipestifer infection

International Common Names

  • English: anatipestifer syndrome; duck septicaemia; duck septicemia; goose influenza; infectious serositis; new duck disease; polyserositis; riemerella anatipestifer in birds, duck septicemia, infectious serositis; riemerellosis; septicaemia; septicemia; serositis; sinusitis

Local Common Names

  • Germany: septicemia anserum exudativa

Overview

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Riemerella anatipestifer infection is a septicaemic (acute, peracute, sometimes chronic) disease of primarily ducks and geese, but it also affects turkeys, chickens, pheasants, guinea fowls, quails and swans. The infection causes serious losses in ducks and geese due to high mortality. It usually occurs in young birds of 1-8 weeks of age. In addition to mortality, it causes carcass condemnation and weight loss. The disease was first reported in the USA in 1932 (Henricksen and Hilbert, 1932) in ducks in an area of intensive duck farming where it was known as ‘new duck disease’. Other synonyms are infectious serositis (Dougherty et al., 1955), anatipestifer syndrome and duck septicaemia. A similar disease in goslings ‘septicaemia anserum exudativa’ was reported by Riemer in 1904. Later, it was known to be caused by the same bacterium that is responsible for the disease in ducklings. R. anatipestifer infection has been reported worldwide.

R. anatipestifer infection is caused by a Gram-negative bacterium named initially as Pfeifferella anatipestifer. Because of its uncertain taxonomic status, it was placed under various genera and named as Moraxella anatipestifer, Pasteurella anatipestifer and species incertae sedis. On the basis of its DNA base composition and cellular fatty acid profile, it was transferred to Flavobacterium-Cytophaga group (Piechulla et al., 1986). Segers et al., (1993) reported significant differences between this organism and other members of Flavobacterium and Weeksella, and suggested the name Riemerella anatipestifer in honor of Riemer (1904) who initially reported the disease ‘septicaemia anserum exudativa’ in geese.

The control of this infection is rather difficult because R. anatipestifer has at least 21 known serotypes, and different serotypes do not provide cross-protection against each other. Very often, more than one serotype are responsible for disease in a flock or on a farm. An effective vaccine has to be multivalent to provide protection against predominant serotypes. The infection can be treated with antibiotics, but is mostly controlled through vaccination. The infection is not of any public health importance, and is not reportable to regulatory authorities.

Hosts/Species Affected

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Riemerella anatipestifer infection is primarily a disease of ducks and geese. It has also been reported in turkeys (Zehr and Ostendorf, 1970; Helfer and Helmboldt, 1977), chickens (Rosenfeld, 1973), pheasants (Bruner et al., 1970), swans (Munday et al., 1970), guinea fowls and quails (Pascucci et al., 1989).

Distribution

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Information given in the Geographical Distribution table shows the occurrence of Riemerella anatipestifer infection in countries that produce ducks, geese and turkeys. The disease is widespread in intensive duck producing areas of China, Thailand, Taiwan, USA, UK, Germany and Hungary. The infection has also been reported from Canada, Denmark, Italy, France, Netherlands and Australia. Sporadic cases have been reported from India, Bangladesh, Singapore, Israel, Korea, Egypt, Russia and New Zealand.

Distribution Table

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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/RegionDistributionLast ReportedOriginFirst ReportedInvasiveReferenceNotes

Asia

BangladeshPresentMustafa et al., 1985
ChinaWidespreadCheng et al., 2003
-AnhuiWidespreadHu et al., 2001
-FujianWidespreadHuang et al., 1999
-GuangdongWidespreadGuo Yujiang, 1983; Gao and Guo, 1988; Zhang et al., 1999
-HebeiWidespreadGao and Guo, 1988; Zhang and Guo, 1999
-JiangsuWidespreadHu et al., 1997
-JiangxiWidespreadZhu et al., 2001
-SichuanWidespreadCai et al., 2001; Wang et al., 2002
-YunnanWidespreadWang et al., 2001
-ZhejiangWidespreadBao et al., 1997; Hu et al., 2003
IndiaPresentMurthy et al., 1981; Sarma et al., 1985
-AssamPresentChaudhury and Mahanta, 1985
-West BengalPresentSadhukhan et al., 2001
IsraelWidespreadBendheim and Even-Shoshan, 1975; Bendheim et al., 1978
JapanPresentSakurai et al., 1987
Korea, Republic ofWidespreadKang and Koh, 1993; Kolodzieyski et al., 2002
SingaporeWidespreadSingh et al., 1982; Loh et al., 1992
TaiwanWidespreadChang, 1984; Huang et al., 1991
ThailandWidespreadMahitanan et al., 1982; Pathanasophon et al., 1994; Kohler et al., 1997

Africa

EgyptPresentBayoumi et al., 1988; Ibrahim et al., 2000

North America

CanadaWidespreadTaylor, 1955; Sandhu and Harry, 1981
-AlbertaPresentLeavitt and Ayroud, 1997
-ManitobaPresentWobeser et al., 1982
-OntarioPresentSandhu and Harry, 1981
-SaskatchewanPresentWobeser and Ward, 1974
USAPresentPresent based on regional distribution.
-CaliforniaWidespreadSmith et al., 1987
-ConnecticutPresentJortner et al., 1969
-IllinoisPresentGraham et al., 1938; Tripathy et al., 1980; Campagnolo et al., 2001
-IndianaWidespreadSandhu and Harry, 1981
-MinnesotaPresentCharles et al., 1991
-New YorkPresentHendrickson and Hilbert, 1932
-OregonPresentHelfer and Helmboldt, 1977
-South CarolinaPresentEleazer et al., 1973
-UtahPresentBrogden et al., 1982

Europe

Czech RepublicPresentRachac and Vladík, 1987
DenmarkPresentBisgaard, 1982; Bisgaard, 1995
FrancePresentSaint et al., 1972; Vallee et al., 1972; Ganiere et al., 1983
GermanyWidespreadRiemer, 1904; Gerlack, 1970; Ziedler et al., 1984; Floren et al., 1987
HungaryWidespreadBitay et al., 1979; Ivanics et al., 1996
ItalyWidespreadPascucci et al., 1981; Giovannetti and Pascuccci, 1983
PolandPresentGazdzinski and Minta, 1978
Russian FederationPresentGoroshko and Prokofeva, 1958
SpainPresentLeon et al., 1980
UKWidespreadAsplin, 1955; Harry, 1969; Timms and Marshall, 1989

Oceania

AustraliaWidespreadMunday et al., 1970; Grimes and Rosenfield, 1972; Rosenfeld, 1973
-New South WalesWidespreadJackson, 1972
-VictoriaPresentReece and Coloe, 1985
New ZealandPresentHemsley, 1996

Pathology

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The infection causes septicaemic lesions in affected birds. The heart, liver and airsacs are covered with a yellowish white exudate consisting of fibrin. Both abdominal and thoracic airsacs have thin layers of dry caseous exudate. Spleen is mottled and kidneys are congested. In females, the oviduct contains caseous plugs. Lungs are rarely involved. Occasionally, caseous lesions in the nasal and infraorbital sinuses are observed (Leibovitz, 1972). Lesions in the nervous system include fibrinous meningitis. Chronic infections in ducks may occur in the joints or skin. Skin lesions are in the form of dermatitis with yellowish exudate seen between fat and skin layers, while the outside of the skin appears spongy like a honeycomb. Lesions in turkeys and chickens are similar but less severe.

Histopathological lesions include fibrinous exudate, infiltrated with mononuclear cells and heterophils on the serous surfaces of pericardium, airsacs and liver capsule. Multinuclear giant cells may be seen in airsacs and skin lesions in chronic cases. The liver cells show cloudy swelling, fatty degeneration and necrosis (Chaudhury and Mohanta, 1985). Mottling of spleen is due to an increase in size and number of germinating lymph follicles. Lesions in the central nervous system include serofibrinous inflammation of cerebral and spinal meninges. Extensive exudate in the ventricular system and leukocytic infiltration of subpial and periventricular brain tissue has been observed.

Diagnosis

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Clinical signs in ducklings and goslings include lethargy, ruffled feathers, anorexia, lagging behind the flock, nasal and eye discharge, greenish diarrhoea, incoordination, falling on their back, paddle their legs, and unable to stand or walk. In later stages, affected birds suffer from convulsions of the head and neck, ataxia before death. Mortality can be as high as 75%.

Affected turkeys appear depressed, dehydrated, lame, and have difficulty walking. Later, the birds become moribund and die. The infection causes low but lingering mortality. Similar clinical signs have been observed in chickens and other birds.

Presumptive diagnosis of Riemerella anatipestifer can be made from flock history, clinical signs and lesions. Nervous signs such as tremors of head and neck, falling on back and difficulty to stand up, incoordination and ataxia are very common in infected ducks and geese. Septicaemic lesions, typically fibrinous pericarditis, perihepatitis, airsacculitis, meningitis and salpingitis are also indicative of this infection, although some of these lesions may also be observed in infections with Pasteurella multocida, Escherichia coli or Streptococcus faecium. Similar nervous signs have also been observed in Salmonella infection in ducklings. Chlamydiosis and Coenonia anatina infection should also be considered in differential diagnosis. Confirmatory diagnosis should be based on isolation and identification of the causative organisms.

R. anatipestifer can be easily isolated from brain, heart blood, airsacs, liver, or oviduct by culturing on trypticase soy agar enriched with 0.05% yeast extract, 5% bovine serum or sheep blood. The organism can be identified by sugar, biochemical and enzymatic reactions.

R. anatipestifer isolates are serotyped by agglutination and agar-gel precipitation reactions (Sandhu and Harry, 1981). Slide agglutination test is performed by mixing a small colony with a drop of antiserum on a glass slide. If the isolate is same serotype as the antiserum, agglutination occurs in a few seconds. Tube agglutination can be done to determine antibody titres in a serum. For agar gel precipitin test, supernatant from a heated culture suspension is used as an antigen against known serotype antisera. Precipitin bands appear in 48-72 h. Antibody titres in sera can also be determined by enzyme-linked immunosorbent assays (Hatfield et al., 1987), which is more sensitive than agglutination tests.

List of Symptoms/Signs

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SignLife StagesType
Digestive Signs / Abnormal colour of stool in birds, white, green, yellow faeces Poultry:Day-old chick,Poultry:Young poultry Sign
Digestive Signs / Anorexia, loss or decreased appetite, not nursing, off feed Sign
Digestive Signs / Diarrhoea Sign
General Signs / Ataxia, incoordination, staggering, falling Sign
General Signs / Discomfort, restlessness in birds Poultry:Day-old chick,Poultry:Young poultry Sign
General Signs / Dysmetria, hypermetria, hypometria Sign
General Signs / Fever, pyrexia, hyperthermia Poultry:Day-old chick,Poultry:Young poultry Sign
General Signs / Inability to stand, downer, prostration Poultry:Day-old chick,Poultry:Young poultry Sign
General Signs / Increased mortality in flocks of birds Sign
General Signs / Lack of growth or weight gain, retarded, stunted growth Poultry:Young poultry Sign
General Signs / Lameness, stiffness, stilted gait in birds Sign
General Signs / Polydipsia, excessive fluid consumption, excessive thirst Poultry:Day-old chick,Poultry:Young poultry Sign
General Signs / Reluctant to move, refusal to move Sign
General Signs / Swelling of the limbs, legs, foot, feet, in birds Sign
General Signs / Torticollis, twisted neck Sign
General Signs / Underweight, poor condition, thin, emaciated, unthriftiness, ill thrift Sign
General Signs / Weakness, paresis, paralysis of the legs, limbs in birds Sign
General Signs / Weight loss Sign
Nervous Signs / Dullness, depression, lethargy, depressed, lethargic, listless Sign
Nervous Signs / Tremor Sign
Ophthalmology Signs / Chemosis, conjunctival, scleral edema, swelling Sign
Ophthalmology Signs / Conjunctival, scleral, injection, abnormal vasculature Sign
Ophthalmology Signs / Conjunctival, scleral, redness Sign
Ophthalmology Signs / Lacrimation, tearing, serous ocular discharge, watery eyes Sign
Respiratory Signs / Coughing, coughs Sign
Respiratory Signs / Mucoid nasal discharge, serous, watery Sign
Respiratory Signs / Purulent nasal discharge Sign
Skin / Integumentary Signs / Ruffled, ruffling of the feathers Poultry:Day-old chick,Poultry:Young poultry Sign
Skin / Integumentary Signs / Soiling of the feathers, vent feathers Poultry:Day-old chick,Poultry:Young poultry Sign

Disease Course

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Ducks and geese usually get infected through the respiratory tract, although infections through a break in the skin have also been reported ( Leibovitz, 1972). Healthy ducklings may carry the organisms in the respiratory tract (Ryll et al., 2001). Cooper (1989) suggested transmission of infection in turkeys may be transmitted by mosquitoes, but the experimental evidence is circumstantial. After respiratory infection, the organisms gain entry into the blood circulation causing bacteraemia and systemic disease. It is not known as to how the organisms produce septicaemic lesions, although fibrinolytic enzymes, haemolysins and lipopolysaccharides have been suggested to be involved (Bangun et al., 1981; Brogden, 1989). The organisms pass through the blood-brain barrier to cause nervous signs and lesions. In most cases, death occurs within 6-12 h after showing clinical signs, although some sick birds may survive for a few more days before death. Recovered birds are stunted in growth. Chronic infections may result in localized infections of joints and/or skin. Experimental infection can be reproduced by subcutaneous, intramuscular, intravenous, intrasinus (infraorbital) or web-pad injections. The incubation period is about 2 to 5 days. Experimental infection through parenteral routes can cause clinical signs and mortality within 24-48 h. An acute form of the disease occurs in young ducklings. Turkeys usually contract the chronic form; susceptible age is 4 to 18 weeks.

Recovered birds become resistant to infection with a homologous serotype. Although protective antigen(s) have not been isolated or identified, cell-free culture filtrate has been shown to provide protection in ducklings (Pathanasophon et al., 1996). Research studies showed that vaccination with a recombinant outer membrane protein was not protective in ducklings against challenge with a homologous serotype ( Huang et al., 2002).

Epidemiology

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Riemerella anatipestifer infection occurs in the respiratory tract through contact with infected birds or premises. The disease can also occur by infection through a break in skin. The birds develop systemic infection through bacteraemia. In chronic cases, the infection is localized in joints and skin. The organisms are shed through nasal or infraorbital sinus secretions aerosolizing the environments and contaminating feeders and drinkers. The infection spreads fast in flocks raised in confined houses and causes high mortality in young ducklings or goslings. There are no seasonal differences in the incidence of disease in ducks. Outbreaks are common in ducks and geese, but incidence in turkeys, chickens and other birds are sporadic. The disease is rare in older birds or breeder ducks. No vector is known, although mosquitoes have been reported to carry R. anatipestifer, and may be a possible mean of transmission in turkeys (Cooper, 1989).

Impact: Economic

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Riemerella anatipestifer causes high economic losses to the duck and goose industries of waterfowl producing countries. The losses are due to mortality, meat condemnation and weight loss. It adds the financial burden to producers of treatment and control measures, including costs of medications, vaccines and labour. Losses in other birds such as turkeys, chickens and others are low to moderate.

Zoonoses and Food Safety

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Riemerella anatipestifer infection does not have any public health significance. The carcasses of birds showing lesions of infection at the time of slaughter are usually condemned or downgraded.

Disease Treatment

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Riemerella anatipestifer infection can be treated with enrofloxacin (50 p.p.m. in drinking water) or subcutaneous/intramuscular injection of penicillin in dosages of 50,000 IU/kg bodyweight (Turbahn et al., 1997; Sandhu and Dean, 1980). Enrofloxacin should be repeated for the next 4 days at levels of 25 p.p.m. Other treatments include novobiocin, lincomycin or sulfadimethoxine-ormetoprim (5:3) in feed. Medications become less effective after prolonged use, due to development of resistant strains. Users should pay attention to the manufacturers’ recommendations regarding usage, particularly in relation to drug withdrawal periods.

Prevention and Control

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Inactivated vaccines have been used to immunize ducklings against Riemerella anatipestifer infection ( Harry and Deb, 1979; Sandhu, 2003). Autogenous inactivated vaccines are commonly used to provide protection. Since more than one serotype may occur in a hatch of ducks at a farm or in an area, vaccines are usually multivalent to provide broad-spectrum protection against major serotypes responsible for the disease. Inactivated vaccines usually consist of bacterial cells grown in broth media and killed with formalin. Some vaccines are oil-emulsified or contain aluminum hydroxide or other adjuvants. Since most ducks are slaughtered at 6-7 weeks of age, adjuvanted vaccines may produce lesions at the site of injections resulting in condemnation of a part of the carcass. Inactivated vaccines are usually administered subcutaneously in the neck at 2 and 3 weeks of age.

A live avirulent vaccine developed against R. anatipestifer serotypes 1, 2 and 5 infection provide significant protection when administered by aerosol to one-day-old ducklings (Sandhu, 1991). Laboratory data showed protection up to 7 weeks of age though in the field some commercial duck farm follow up with an inactivated vaccine at 2-4 weeks of age. Progeny of breeder ducks vaccinated with an inactivated or live vaccine are protected up to 2-3 weeks of age through maternal immunity.

Management and sanitation play a major role in the prevention of infection. Ducklings maintained under stressful conditions are predisposed to R. anatipestifer infections. Sanitation in a house with confined rearing of multiple-aged flocks is very critical. The whole house should be depopulated for a major clean and disinfection.

References

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Bangun A; Tripathy DN; Hanson LE, 1981. Studies of Pasteurella anatipestifer: An approach to its classification. Avian Diseases, 25:326-337.

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Bendheim U; Even-Shoshan A, 1975. Survival of Pasteurella multocida and Pasteurella anatipestifer in various natural media. Refuah Veterinarith, 32:40-46.

Bendheim U; Even-Shoshan A; Baroutchieva M; Plesser O, 1978. Pasteurella anatipestifer, a pathogenic agent in turkeys: etiology, epizootology and pathogenicity. Proceedings and Abstracts of the XVI World’s Poultry Congress, Volume IX, Rio de Janeiro, Brazil, 1461-1472.

Bisgaard M, 1982. Antigenic studies on Pasteurella anatipestifer, species incertae sedis, using slide and tube agglutination. Avian Pathology, 11:341-350.

Bisgaard M, 1995. Salpingitis in web-footed birds: prevalence, aetiology and significance. Avian Pathology, 24(3):443-452; 12 ref.

Bitay Z; Kovacs G; Takacs G; Torok L, 1979. Occurrence of the anatipestifer syndrome in ducks in Hungary. Magyar (llatorvosok Lapja, 34:747-750.

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Brogden KA, 1989. Pasteurella anatipestifer infection. In: Adam C, Rutter JM, eds. Pasteurella and Pasteurellosis. London, UK: Academic Press, 115-129.

Brogden KA; Rhoades KR; Rimler RB, 1982. Serologic types and physiologic characteristics of 46 avian Pasteurella anatipestifer cultures. Avian Diseases, 26:891-896.

Bruner DW; Angstrom CI; Price JI, 1970. Pasteurella anatipestifer infection in pheasants. A case report. Cornell Veterinarian, 60:491-494.

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Campagnolo ER; Banerjee M; Brundaban Panigrahy; Jones RL, 2001. An outbreak of duck viral enteritis (Duck Plague) in domestic Muscovy ducks (Cairina moschata domesticus) in Illinois. Avian Diseases, 45(2):522-528; 21 ref.

Chang CF, 1984. Pathogenesis of Pasteurella anatipestifer infection in ducks and drug sensitivity. Taiwan Journal of Veterinary Medicine and Animal Husbandry, No. 43:40-46; 17 ref.

Charles SD; Nagaraja KV; Halvorson DA; Rao A, 1991. A retrospective analysis on the epizootiological aspects of outbreaks of Pasteurella anatipestifer infection in turkeys in Minnesota. Poultry Science, 70(8):1704-1708; 15 ref.

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Eleazer TH; Blalock HG; Harrell JS; Derieux WT, 1973. Pasteurella anatipestifer as a cause of mortality in semiwild pen-raised mallard ducks in South Carolina. Avian Diseases, 17:855-857.

Euzéby JP, 2000. The genera Riemerella and Coenonia: a short review. Revue de Médecine Vétérinaire, 151(1):63-68; 11 ref.

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Ganiere JP; Brocas J; Prudhomme M; Villate D, 1983. Demonstration of Pasteurella anatipestifer infection in ducks and geese in France. Revue de Médecine Vétérinaire, 134(12):713-717; 25 ref.

Gao F; Guo YP, 1988. Studies of the vaccine against infectious serositis in ducklings. 1. Serotyping of Pasteurella anatipestifer in China. 2. Preliminary studies of the inactivated bacterins against Pasteurella anatipestifer.. Waterfowl production. Proceedings of the International Symposium, September 11-18, 1988, Beijing, China., 318-327; 10 ref.

Gao F; Guo YP; Wang ZP; Wu ZD, 1989. Epidemiological investigation of the duckling infectious serositis in Shanghai area. Waterfowl production. Proceedings of the International Symposium, September 11-18, 1988, Beijing, China., 370-373; 6 ref.

Gazdzinski P; Minta Z, 1978. Outbreak of infectious serositis in ducks. Medycyna Weterynaryjna, 34:202-204.

Gerlack H, 1970. Pasteurella anatipestifer infektion bei entenk(ker. Deutsche Tierarztliche Wochenschrift, 77:541-542.

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Goroshko IN; Prokofeva MI, 1958. An infectious disease of the respiratory organs of ducks.Veterinariya Moscow, 35:65-69.

Graham R; Brandly CA; Dunlap GL, 1938. Studies on duck septicemia. Cornell Veterinarian, 28:1-8.

Grimes TM; Rosenfield LE, 1972. Pasteurella anatipestifer infection in ducks in Australia. Australian Veterinary Journal, 48:367-368.

Guo Yujiang, 1983. Studies of anatipestifer syndrome of young ducks. Journal of South China Agricultural College, 4(2):11-21; 18 ref.

Harry EG, 1969. Pasteurella (Pfeifferella ) anatipestifer serotypes isolated from cases of anatipestifer septicaemia in ducks. Veterinary Record, 84:673.

Harry EG, 1974. Pasteurella anatipestifer: its characteristics and pathogenicity for ducks. Index to Theses 1971-72 (published 1974), 22:230. London University, UK: PhD Thesis.

Harry EG; Deb JR, 1979. Laboratory and field trials on a formalin inactivated vaccine for the control of Pasteurella anatipestifer septicaemia in ducks. Research Veterinary Science, 27:329-333.

Hatfield RM; Morris BA; Henry RR, 1987. Development of an enzyme-linked immunosorbent assay for the detection of humoral antibody to Pasteurella anatipestifer. Avian Pathology, 16(1):123-140; 19 ref.

Helfer DH; Helmboldt CF, 1977. Pasteurella anatipestifer infection in turkeys. Avian Diseases, 21:712-715.

Hemsley LA, 1996. Duck diseases in New Zealand. Surveillance (Wellington), 23(4):28; 22 ref.

Hendrickson JM; Hilbert KF, 1932. A new and serious septicemic disease of young ducks with a description of the causative organism, Pfeifferella anatipestifer, N. S. Cornell Veterinarian, 22:239-253.

Hinz KH; Ryll M; Köhler B, 1998. Detection of acid production from carbohydrates by Riemerella anatipestifer and related organisms using the buffered single substrate test. Veterinary Microbiology, 60(2/4):277-284; 19 ref.

Hu JH; Sun FP; Wang Y; Liu HY; Wu ZL, 2003. Isolation of Riemerella anatipestifer and its immune protection. Acta Agriculturae Shanghai, 19:109-111.

Hu QH; Li G; Zheng MQ; Cai BX, 1997. Isolation and identification of Pasteurella anatipestifer. Chinese Journal of Veterinary Science and Technology, 27:22-24.

Hu QingHai; Zhang ZhiLiang; Miao JinFeng; Liu YueLong; Liu XiaoWen; Ding Chan, 2001. Epidemiologic investigation of Riemerella anatipestifer infection in ducks in Jiangsu and Anhui provinces. Chinese Journal of Veterinary Science and Technology, 31(8):12-13; 2 ref.

Huang Bin; Subramaniam S; Frey J; Loh H; Tan HaiMeng; Fernandez CJ; Kwang J; Chua KimLee, 2002. Vaccination of ducks with recombinant outer membrane protein (OmpA) and a 41 kDa partial protein (P45N) of Riemerella anatipestifer. Veterinary Microbiology, 84(3):219-230; 31 ref.

Huang HT; Hsu HS; Chuang CT; Tsung TM; Chen WL; Hung HH; Chang RR, 1991. Infectious serositis in waterfowl in Pingtung county: pathogen isolation, gross and histological lesions, and serum agglutinating antibody analysis. Taiwan Journal of Veterinary Medicine and Animal Husbandry, No.57:63-70; 12 ref.

Huang Y; Li WY; Cheng LF; Su JL; Lu YL, 1999. First isolation and identification of Riemerella anatipestifer type II in Fujian Province, China. Journal of Fujian Academy of Agricultural Sciences, 14:43-46.

Ibrahim RS; Sohair; Hussein Z, 2000. Bacterial agents associated with sinusitis in waterfowls and turkeys in Assiut and El-Minia Governorates. Assiut Veterinary Medical Journal, 44(87):185-195; 24 ref.

Ivanics é; Glávits R; Edés I, 1996. Study in Pasteurella anatipestifer infection in young geese. Magyar állatorvosok Lapja, 51(1):9-14; 14 ref.

Jackson CAW, 1972. Suspected Pasteurella anatipestifer infection in ducklings in New South Wales. Australian Veterinary Journal, 48:479.

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