Nguyen Pham Thao Nhi, Tran Duy Thanh,

Nguyen Khanh Thuan, Nguyen Phuc Khanh, Nguyen Thanh Lam*

1. Introduction

Riemerella anatipestifer (RA) infection is also known as new duck disease, duck septicemia, anatipestifer syndrome, anatipestifer septicemia, and infectious serositis. In geese, R. anatipestifer  infection has been called goose influenza or septicemia anserum exsudativa (Levine 1965). It affects both ducks and geese, and occurs as an acute or chronic septicemia characterized by fibrinous pericarditis, perihepatitis, airsacculitis, caseous salpingitis, and meningitis. Riemerella columbina (RC), a similar organism to R. anatipestifer , has been isolated from clinically diseased pigeons (Rubbenstroth, Hotzel et al. 2011).

R. anatipestifer infection is a major disease confronting the duck industry worldwide. It accounts for significant economic losses because of high mortality, weight loss, condemnations, downgrading, and salvage. Prevention and control programs consist of diagnosing the infection, vaccinating at‐risk flocks, and treating the disease, which all add to the production cost.

The disease has no public health significance (McMullin 2020).

2. Aetiology

2.1 Bacteria characteristics

R. anatipestifer is a member of the Flavobacteriaceae family. It is a Gram-negative bacteria, nonmotile, nonspore‐forming rod that occurs singly, in pairs, and occasionally in chains. The cells vary from 0.2 to 0.4 mm in width and 1 to 5 mm in length. Many cells stain bipolar with Wright’s stain, and a capsule can be demonstrated in preparations with India ink (McMullin 2020). There are 21 known serotypes and infection is spread horizontally between birds. Infection may be referred to as Duck Septicaemia, Goose’ flu, Riemerellosis, New Duck Disease and Polyserositis.

Virulence factors

Several R. anatipestifer  virulence factors have been identified that associate with disease severity, including VapD (Chang, Hung et al. 1998), CAMP cohemolysin (Crasta, Chua et al. 2002), outer membrane protein A (OmpA) and P45 (Hu, Han et al. 2011), nicotinamidase PncA (Wang, Liu et al. 2016), and putative genes associated with lipopolysaccharide (LPS) synthesis. In addition, (Wang, Lu et al. 2017) studied the fact that two‐component signaling systems (TCS), a basic stimulus‐response coupling mechanism for some bacteria, regulates gene expression and virulence in R. anatipestifer.

2.2 Classification

Originally called Pfeifferella anatipestifer (Hendrickson and Hilbert 1932) then Moraxella anatipestifer (Bruner and Fabricant 1954), it was finally listed in the 7^th edition of Bergey’s Manual of Determinative Bacteriology as Pasteurella anatipestifer(Sandhu 2008). However, because of its uncertain taxonomic status, R. anatipestifer  was placed as species incertae sedis in the 8th (Sandhu 2008) and 9th (Mannheim, Carter et al. 1984) editions of Bergey’s Manual of Systematic Bacteriology.

Comparison of DNA‐base composition, DNA‐DNA homology, and cellular fatty‐acid profile indicated it should be excluded from the genus Moraxella as well as Pasteurella (Bangun, Johnson et al. 1987). Suggestions to transfer R. anatipestifer to the Flavobacterium/Cytophaga group was made based on its low but significant DNA binding and ability to produce menaquinones and branched‐chain fatty acids (Piechulla, Pohl et al. 1986). However, given significant differences between R. anatipestifer  and its close genotypic relatives Flavobacterium and Weeksella (Segers, Mannheim et al. 1993), it was suggested that a separate genus should be created, Riemerella, in honor of Riemer (Riemer 1904), who first described the disease “septicemia anserum exsudativa” in geese in 1904. It was ultimately named R. anatipestifer on the basis of DNA‐ribosomal RNA hybridization analysis, protein and fatty acid methylester (FAME) profiles, and phenotypic characteristics such as lack of pigment production and presence of the respiratory quinone, menaquinone.

R. anatipestifer‐like organisms of taxon 1502 (Hinz, Ryll et al. 1998) isolated from ducks and geese were assigned to the genus Coenonia and named Coenonia anatina gen. nov., sp. nov. on the basis of its phenotypic and genotypic characteristics and FAME profiles (Vandamme, Vancanneyt et al. 1999). C. anatinadiffers from R. anatipestifer by the absence of arginine dihydrolase and gelatinase and by the presence of hyaluronidase, chondroitin sulfatase activity, aesculin hydrolysis, and b‐glucosaminidase activity. Genome sequences of R. anatipestifer  strains ATCC 11845, R. anatipestifer‐GD, and R. anatipestifer‐YM, have been published (Mavromatis, Lu et al. 2011).

3. History

R. anatipestifer infection was first described in 1932 in Pekin ducks from three farms on Long Island, New York (Hendrickson and Hilbert 1932). The report referred to a new disease, which became known in the area as “new duck disease”. The disease started in 7- to 10-week-old ducks with about 10% mortality and later spread to younger ducklings of about 3 weeks of age. Six years later, the disease was observed in ducks from a commercial farm in Illinois and was reported as “duck septicemia” (Graham, Brandly et al. 1938). The designation “infectious serositis” was given by Dougherty and coworkers after (Dougherty 3rd, Saunders et al. 1955) a comprehensive pathologic study. The term R. anatipestifer infection was recommended by (Leibovitz 1972) to identify the disease specifically caused by R. anatipestifer and to differentiate it from other infections with similar pathology. A similar disease, septicemia anserum exsudativa, was described in geese. The causative agent, Pasteurella septicaemiae, is identical to R. anatipestifer on the basis of reported characteristic (Sandhu, 2008).

4. Epidemiology

4.1 Geographic distribution

R. anatipestifer infection occurs worldwide and has been recognized in countries that have intensive duck production (Sandhu 1986). R. anatipestifer  pathogenic infections in domestic ducks (Anas platyrhynchos) have been recently reported in Japan (Chikuba, Uehara et al. 2016). Wide variation has been observed in the severity of the disease depending on the strain of the organism, age of the host and route of exposure. Often, more than one serotype is responsible for the disease at a single farm or in the same hatch of birds (McMullin 2020).

4.2 Susceptible hosts

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

Table 1. Animals host (https://www.cabi.org/isc/datasheet/66183)

4.3 Transmission

Infection takes place via the birds’ respiratory tract or through skin wounds, particularly on the feet. R. anatipestifer  and R. anatipestifer‐like bacteria have been isolated from pharyngeal mucosa of clinically normal ducklings. Cooper suggested that in turkeys, the disease may be transmitted via arthropod vectors based on its seasonal occurrence and the apparent affinity of R. anatipestifer for host erythrocytes. The disease can be reproduced most consistently by injecting the organism intravenously, subcutaneously, intraperitoneally, intramuscularly, in the foot pad, or in the infraorbital sinus. Experimental infection by subcutaneous and intravenous routes caused high mortality, whereas no or low mortality was observed in ducklings infected by the oral or nasal route (McMullin 2020)

5. Clinical signs and pathology 

5.1 Clinical signs

Signs most often observed are listlessness, ocular and nasal discharge, mild coughing and sneezing, greenish diarrhea, ataxia, torticollis, tremor of head and neck, and coma (Figure 5).

Affected ducklings lie on their backs paddling with their legs and are unable to move. Surviving ducks may be stunted (Pickrell 1966). Adverse environmental conditions or concomitant disease often predispose birds to outbreaks of R. anatipestifer infection. Mortality may vary from 5% to 75%; morbidity is usually higher.

5.2 Pathology

Gross

The most obvious gross lesion in ducks is fibrinous exudate, which involves serosal surfaces in general, but is most evident on the pericardium, and air sacs (Figure 6). Similar lesions have been reported in turkeys and other birds. Fibrinous airsacculitis is common; both abdominal and thoracic air sacs may be involved. The spleen may be enlarged and mottled. Mucopurulent exudate in nasal sinuses and caseous exudate in oviducts also have been observed.

Chronic localized infections may occur under the skin and occasionally in the joints. Skin lesions usually take the form of necrotic dermatitis on the lower back or around the vent. Yellowish exudate has been observed between layers of the skin and fat.

Microscopic

Fibrinous exudate on the heart contains a few inflammatory cells, primarily mononuclear cells, and heterophils. In acute cases, severe focal necrosis of the heart muscle is present (Figures 7 and 8). Liver lesions observed in the acute stage of the disease are mild periportal mononuclear leukocytic infiltration, cloudy swelling, and hydropic degeneration of parenchymal cells. In less acute cases, moderate periportal lymphocytic infiltration may be observed. In air sacs, mononuclear cells are the predominant cell type in the exudate. Multinuclear giant cells and fibroblasts may be observed in chronic cases. The respiratory tract also may be infected without showing clinical signs. The lungs of infected ducks may be unaffected; there may be interstitial cellular infiltration and proliferation of lymphoid nodules adjacent to parabronchi, or there may be an acute fibrinopurulent pneumonia. Infections of the central nervous system can produce fibrinous and lymphocytic meningitis (Figure 9). Jortner, Porro et al. 1969 studied lesions in the central nervous system of naturally infected ducklings and described diffuse fibrinous meningitis with leukocytic infiltration in and around the walls of meningeal blood vessels.

Extensive exudate was observed in the ventricular system. Slight to moderate leukocytic and microglial infiltrates were observed in subpial and periventricular brain tissue. Lymphoid necrosis and depletion of lymphocytes have been observed in the spleen and cloacal bursa. Biofilm formation has been described as a contributing factor in persistent R. anatipestifer  infections (McMullin 2020).

Immunity

Ducklings that recover from the disease are resistant to subsequent infection. Inactivated bacterins have been used in ducks to prevent R. anatipestifer infection. Ducks vaccinated with formalin‐inactivated bacterins and sub-sequently challenged with strains representing serotypes 1, 2, and 5 developed homologous, but not heterologous, protection. A trivalent bacterin containing these strains protected against challenge with each serotype, but the protection lasted only a short time. Harry and Deb 1979 evaluated the effectiveness of several types of bacterins and conducted a field trial with a formalin inactivated bacterin. A single dose of oil‐emulsion bacterin provided longer lasting immunity in ducklings.

Cell‐free culture filtrate also has been reported to provide significant protection against homologous challenge. Outer membrane proteins OmpA and P45 failed to protect against a virulent challenge, but produced R. anatipestifer‐specific antibodies. One‐day‐old ducklings exposed to live avirulent strains by aerosol or through the drinking water were resistant when challenged at 3–6 weeks of age with virulent homologous strains. Passive protection of progeny can be achieved by immunizing the female breeder ducks; maternal immunity lasts for about 2–3 weeks. R. anatipestifer‐specific antibodies were detected in the egg yolk and sera of vaccinated breeder ducks; maternal antibodies in the progeny lasted up to 10 days of age. Cell‐mediated immunity to R. anatipestifer  antigens was transient (similar to vaccination with the bacterin), and live vaccine induced longer lasting protection. Harry and Deb 1979 identified and described an immunogenic protein, chaperonin GroEL, from the outer membrane of R. anatipestifer strain WJ4 using an immunoproteomic assay based on matrix‐assisted laser desorption/ionization time of flight mass spectrometry. They found that the groEL gene is highly conserved among R. anatipestifer  strains; indeed, the DNA sequence identity was more than 97.5% between WJ4 and the 9 additional R. anatipestifer  strains. Fernandez, Kim et al. 2016 described the importance of interleukin‐17A (IL‐17A) in the pathogenesis of R. anatipestifer  infections in ducks (McMullin 2020). 

6. Diagnosis

Isolation and identification of the causative agent

Although a presumptive diagnosis may be made from clinical signs and necropsy findings, a definite diagnosis should be based on isolating and identifying R. anatipestifer. The bacterium can be isolated most readily when birds are in the acute stage of the disease. Suitable tissues for culture are the brain, blood from the heart, air sacs, bone marrow, lungs, liver, and exudates from lesions. Samples should be taken aseptically, streaked on blood agar or trypticase soy agar containing 0.05% yeast extract, and incubated in a candle jar at 37°C for 24–72 hours. Adding newborn calf serum (5%) and gentamicin (5mg/1,000 mL) to plate media is helpful for isolating R. anatipestifer from contaminated specimens. Isolated colonies should be selected for inoculation of the differential media and identified on the basis of characteristics described in “Etiology.” Serotype identification can be established by agglutination and/or AGP reactions with specific antisera. Molecular fingerprinting by restriction endonuclease analysis and repetitive sequence PCR are useful to differentiate R. anatipestifer strains and may be helpful in epidemiological studies. Using PCR amplifying 16S rDNA has been reviewed by (Qu, Cai et al. 2006). A rapid assay for detecting R. anatipestifer has been developed based on the groEL and ompA genes sequence of R. anatipestifer using LAMP. In addition, Huang, Subramaniam et al. 1999 developed a multiplex polymerase chain reaction (m‐PCR) that discriminates R. anatipestifer , Escherichia coli, and Salmonella enterica in clinical samples from diseased ducks. Colloidal gold immunochromatographic strips have been used for detection of R. anatipestifer  (McMullin 2020).

Serology

Immunofluorescent procedures can be used to identify R. anatipestifer in tissue or exudate from infected birds. Agglutination tests and ELISA can be used to detect serum antibodies. ELISA is more sensitive than agglutination tests but is not serotype‐specific (McMullin 2020).

 Differential diagnosis

R. anatipestifer infection should be differentiated from other septicemic diseases caused by Pasteurella multocida, Coenonia anatina, Escherichia coli, Streptococcus faecium, and salmonellae. Because these diseases produce gross lesions indistinguishable from those caused by R. anatipestifer, diagnosis must include isolation and identification of the causal organism. Differential diagnosis should also include chlamydiosis, especially in turkeys and in areas where the latter is a serious problem (Sandhu 2008).

7. Treatment

Antibiotics and sulfa drugs have been tested for treatment of R. anatipestifer with varying degrees of success. Sulfamethazine, 0.2–0.25%, in drinking water or feed, was reported to prevent the onset of clinical signs in ducks exposed experimentally to R. anatipestifer (Asplin 1955). Sulfaquinoxaline at levels of 0.025 or 0.05% in feed was effective in reducing mortality in field and experimental infections (Sandhu and Dean 1980). Medicated feeds containing novobiocin (0.0303– 0.0368%) or lincomycin (0.011–0.022%) were reported to be highly effective in reducing mortality when started 3 days prior to experimental infection. A combination of sulfadimethoxine and ormetoprim, when administered at 0.02–0.12% levels in feed, prevented or reduced mortality and gross lesions in experimentally exposed ducks (Mitrovic, Schildknecht et al. 1980). Tetracyclines were of little value for treatment of R. anatipestifer  infection  (Sandhu and Dean 1980). Subcutaneous injection of lincomycin-spectinomycin, penicillin, or a combination of penicillin and dihydrostreptomycin were reported to be effective in reducing mortality in artificially infected ducklings (Sandhu and Dean 1980). Enrofloxacin has been shown to be highly effective in preventing mortality in ducklings when given in drinking water at levels of 50 ppm for the first day followed by 25 ppm for the next 4 days (Turbahn, De Jäckel et al. 1997). Ceftiofur, a broad-spectrum cephalosporin, reduced mortality in experimentally infected ducklings given a single dose of 2 mg/kg bodyweight subcutaneously 5 hours after infection (Chang, Lin et al. 2003).

• Injectable solution

100ml CEPTIFI SODIUM or CEPTRISUL OR CEQUIN P+S + 20ml CHYMOSIN FORT  + 40ml VIMEKAT for 1ml/1,2kg of bodyweight 

• Oral administration

+ VIMENRO: 1g/4kg of body weight or 2.5g/1liter of water/ day or 5g mix 1kg of feed

+ CHYMOSIN FORT: 1ml/liter of water/day

+ TYLOFOS: 1g/ 20kg of boddyweight

• Immune system booster supplement

+PROBISOL: 1G/10KG of bodyweight or 1g/ 0.5 kg of feed

+VIME C ELECTROLYTE: 

+ VIMEKAT PLUS: 4-6ml/ liter of water, for 3-5 consecutive days. 

8. Control and prevention of R. anatipestifer 

8.1 Control and prevention

Inactivated vaccines have been used to immunize ducklings against R. anatipestifer infection (Harry and Deb 1979). 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.

8.2 Vaccination

Inactivated bacterins have been reported to prevent or reduce mortality due to R. anatipestifer. Because immunity induced by bacterins is serotype-specific, an ideal bacterin should contain cells of the predominant serotypes to provide an effective protection. A bacterin containing serotypes 1, 2, and 5 has been used in the United States and Canada. Ducklings are vaccinated at 2 and 3 weeks of age to provide adequate protection up to market age (Layton and Sandhu 1984). A single inoculation of oil-emulsified bacterin has been reported to produce longer-lasting protection, but it may cause unfavorable lesions at the site of inoculation.

A live R. anatipestifer vaccine, developed against serotypes 1, 2, and 5, provided significant protection against experimental or field infections with virulent organisms when administered to 1-day-old ducklings by aerosol or in drinking water (Sandhu 1991). A single vaccination protected ducklings up to at least 42 days of age. The vaccine strains grew in the upper respiratory tract and produced a humoral antibody response. The vaccine was demonstrated to be avirulent to 1-day-old ducklings when administered by aerosol or injection into the infraorbital sinus. The vaccine strains were safe in ducks up to 10 back-passages using the contact-exposure method. Breeder ducks can be vaccinated with the bacterin or live vaccine to provide protection in progeny through maternal immunity that may last up to 2–3 weeks of age. Maternally immune ducklings respond successfully to active immunization with a live or inactivated vaccine (Sandhu 2008).

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