Ornithobacterium rhinotracheale infection

International Common Names

• English: ornithobacterium rhinotracheale infection in turkeys and chickens

In 1994, Vandamme et al. proposed that a bacterium isolated from the avian respiratory tract should be assigned to a new genus, Ornithobacterium. The type species of the genus, Ornithobacterium rhinotrachelae, is the only species that has been described so far, but genetic investigation has revealed that more species or subspecies probably exist within the genus (van Empel and Hafez, 1999). O. rhinotrachelae is positioned in the taxonomic tree near the genera Flavobacterium, Cytophaga, Capnocytophaga and Riemerella within rRNA superfamily V (Vandamme et al., 1994). Athough not officially described until 1994, investigations of culture collections have revealed that the bacterium was first isolated in 1981 from turkeys with respiratory disease in Germany, and then in 1983 from rooks in Germany.

A new respiratory disease of poultry associated with O. rhinotracheale was reported in the early 1990s. Respiratory problems, together with purulent pneumonia, airsacculitis, severe growth retardation and increasing mortality were reported in meat turkeys and broilers in South Africa, Germany, the USA, France and the Netherlands (Charlton et al., 1993; Léorat et al., 1994; van Beek et al., 1994; Hafez et al., 1996). A slow growing, pleomorphic, gram-negative rod was repeatedly isolated from affected organs. Initially, this new bacterium was named Pasteurella-like, Kingella-like or ‘taxon 28’ (van Beek et al., 1994). Vandamme et al. (1994) proposed the name Ornithobacterium rhinotracheale gen. nov. sp. nov. after investigating a collection of isolates from the respiratory tracts of turkeys, chickens, rooks and a partridge in France, Belgium, Germany, South Africa, the USA and UK.

The disease caused by O. rhinotracheale has been reproduced experimentally in both chickens and turkeys. In early experiments not all of the clinical signs could be reproduced without priming with a virus (van Empel et al., 1996). These findings resulted in speculation that O. rhinotracheale is not a primary pathogen. However, using O. rhinotracheale alone, Sprenger et al. (1998) experimentally produced the clinical disease, mortality and pathology in male turkeys that resembled that of field infections. Van Veen et al. (2000b) was able to induce lesions in broilers after aerosol challenge with O. rhinotracheale without priming with virus, showing that O. rhinotracheale is also a primary pathogen in chickens.

O. rhinotracheale now has a worldwide distribution in commercial poultry (van Empel and Hafez, 1999) and it affects birds of all ages. It has been associated with hatching problems of chicken and turkey eggs (El-Gohary, 1998). It has also been associated with disease in broilers (van Beek et al., 1994; Sakai et al., 2000; van Veen et al., 2000a), meat turkeys (Hinz et al., 1994; van Beek et al., 1994; Zorman-Rojs et al., 2000), layers, broiler breeders and turkey layers (Joubert et al., 1999; Sprenger et al., 2000a).

The most common post-mortem findings observed in clinical outbreaks and after experimental infection are airsacculitis and pneumonia. Other findings include tracheitis, pericarditis, sinusitis and pleuritis (Charlton et al., 1993; Hinz et al., 1994; van Beek et al., 1994; van Empel et al., 1996; El-Gohary and Awaad, 1998; Roepke et al., 1998; Sakai et al., 2000; van Veen et al., 2000a).

Histopathological examination of infected broilers reveals infiltration of the lungs and air sacs by lymphocytes and polymorphonuclear heterophils (van Veen et al., 2000a). The lumen of these organs contains masses of fibrinopurulent exudates. In the muscles, some diffuse loss of cross-striation, indicative of degenerative changes may be seen. Lymphocytes accumulate in the liver. Using peroxidase-antiperoxidase staining, van Veen et al. (2000a) found that O. rhinotracheale antigen was abundant in the respiratory organs and also in the tendons, not only in the tendon sheath, but in the aponeurosis to the bone as well.

In turkeys, prominent post-mortem lesions include serofibrinous bronchopneumonia with blood in the trachea and bronchi, and a fibrinous inflammation of the thoracic airsacs (Hinz et al., 1994). The lungs are swollen, congested, heavy and consolidated (Abdul-Aziz and Weber, 1999). Histopathological examination reveals severe fibrinoheterophilic inflammation in the airways, pleura and air sacs, and severe perivascular interstitial oedema in the lungs (de Rosa et al., 1996). In the liver there is acute coagulative necrosis of hepatocytes, associated with occasional thrombosis at the periphery of the liver lobes.

After experimental infection of male turkeys (22 weeks old), Sprenger et al. (1998) found that the lungs were reddened, wet and heavy, failed to collapse, and were covered by tenacious tan-to-white exudates. Microscopically, the parabronchi and air capillaries were filled with fibrin, heterophils, macrophages and small numbers of gram-negative bacteria. The pleura was often covered by a thick layer of fibrin, heterophils and macrophages. O. rhinotracheale was recovered from the lungs of most birds with pneumonia and was also cultured from the air sacs, sinuses, trachea, spleen and liver.

O. rhinotracheale infections are characterized by respiratory disease, together with growth retardation and increased mortality rates (Charlton et al., 1993; van Beek et al., 1994; van Empel and Hafez, 1999). Osteitis, meningitis and joint infections, which can be induced by intravenous application, have also been associated with O. rhinotracheale (van Beek et al., 1994; van Empel and Hafez, 1999). Airsacculitis and pneumonia are the most common features of an O. rhinotracheale infection (van Empel and Hafez, 1999).

O. rhinotracheale has been associated with hatching problems in chicken and turkey eggs (El-Gohary, 1998). The bacterium has been isolated from infertile eggs, dead embryos, dead-in-shell chickens and turkeys, and day-old chicks and turkey poults.

In broilers, clinical signs may appear from as early as 2 weeks of age (van Beek et al., 1994), and last until the end of the fattening period (van Beek et al., 1994; Sakai et al., 2000; van Veen et al. 2000a). Clinical signs include a reduction in growth, coughing, sinusitis, sneezing, nasal discharge and lacrimation (van Veen et al., 2000a). Diarrhoea with green faeces, and head tremors have also been reported (Sakai et al., 2000). The mortality rate varies from 1% to more than 10% (van Beek et al., 1994; Hafez, 1996; Sakai et al., 2000; van Veen et al. 2000a). In broiler breeders, O. rhinotracheale has been associated with a decreased egg production of 10 to 38%, at 30 to 38 weeks of age (Youssef and Ahmed, 1996). The birds had mild respiratory symptoms, depressed food intake and increased mortality. Their eggs were small, colourless and had a soft-shell. Infections have occasionally been reported in layers (Sprenger et al., 2000a).

In meat turkeys, O. rhinotracheale infection has been reported at 2-8 weeks of age (van Beek et al., 1994), but disease tends to occur from approximately 14 to 26 weeks of age (Hinz et al., 1994; Amonsin et al., 1997; Abdul-Aziz and Weber, 1999; Roepke et al., 1998). Infection with O. rhinotracheale has been associated with fibrinopurulent pneumonia, and sinusitis, tracheitis, hepatomegaly, splenomegaly, pericarditis and facial oedema have also been observed (Hafez, 1996; Back et al., 1998b). Clinical signs include weakness, dyspnoea, gasping and expectoration of blood-stained mucus (Charlton et al., 1993; Hinz et al., 1994; Back et al., 1998b). Cyanosis of the bare area of the head has also been reported (Hinz et al., 1994). Young (10-day-old) turkeys experimentally infected with O. rhinotracheale exhibited shivering, crowding, rhinitis, dyspnoea and apathy (Ryll et al., 1996). Decreased weight gain has been observed in field outbreaks and after experimental infection (Abdul-Aziz and Weber, 1999; Roepke et al., 1998; Sprenger et al., 1998). A mortality rate of 1 to 7% has typically been reported for turkeys (Hinz et al., 1994; Amonsin et al., 1997; Abdul-Aziz and Weber, 1999; Lombardi et al., 1999), although it can reach higher than 10% (Back et al., 1998b). Under field conditions, older turkeys (16 to 24 weeks old) appear to suffer more severely than younger birds (Hinz et al., 1994). Roepke et al. (1998) found that the severity of clinical signs and mortality increased with age. In turkey layers, a severe respiratory disease with an increased mortality rate and a significant drop in egg production has been found at 52 weeks of age (Joubert et al., 1999).

Early attempts at experimentally infecting chickens and turkeys by intra-air sac or aerosol administration of O. rhinotracheale reproduced some, but not all, of the clinical signs observed in clinical outbreaks (van Empel et al., 1996). Clinical signs seen in outbreaks, such as weakness, dyspnoea, mucus discharge and mortality were not observed after experimental infection (van Empel et al., 1996). It has been suggested that this discrepancy between natural and experimental O. rhinotracheale infection might be explained by differences in predisposing and aggravating factors. Turkey rhinotracheitis virus has been found to have a triggering effect on O. rhinotracheale infection in turkeys (van Empel et al., 1996). Newcastle disease virus (NDV), and to a lesser extent, infectious bronchitis virus, have been found to have triggering effects on O. rhinotracheale infection in chickens (Travers 1996; van Empel et al., 1996; van Empel et al., 1999). Under field conditions, other factors can also be of importance such as stress, high stocking density, poor ventilation, presence of other bacteria or high ammonia levels.

Sprenger et al. (1998) reported the first experimental production of clinical disease, mortality and pathology resembling that of field infections by using O. rhinotracheale alone. Within 24 h after intratracheal inoculation, turkeys (22-week-old males) were depressed, coughing and had decreased feed intake. By 48 h, several birds were coughing up blood and died. Turkeys that survived to day 7 after inoculation had severe, subacute pneumonia. Van Veen et al. (2000b) were able to induce lesions in chickens after aerosol challenge with O. rhinotracheale without priming with virus, showing that O. rhinotracheale is a primary pathogen in chickens.

O. rhinotracheale is found in wild birds as well as chickens and turkeys (Vandamme et al., 1994). In order to determine the molecular epidemiology of O. rhinotracheale, Amonsin et al. (1997) characterized 55 isolates from poultry and wild birds from eight countries on four continents. They found that the majority of O. rhinotracheale isolates recovered from domesticated poultry throughout the world are represented by a small group of closely related clones. Virtually all the O. rhinotracheale isolates recovered from poultry were assigned to the ET 1 complex. In contrast, none of the four isolates from rooks or guinea fowl were assigned to the common ET 1 complex. The paucity of variation in O. rhinotracheale isolates from domesticated poultry suggests that this organism has had a relatively short evolutionary history in this population. The available evidence suggests that the bacterium was recently introduced to domesticated poultry from the wild bird populations.

O. rhinotracheale can be transmitted horizontally by aerosol (van Empel and Hafez, 1999). The occurrence of O. rhinotracheale infections in birds at an early age (Léorat et al., 1994; van Beek et al., 1994), and the presence of maternally-derived antibodies in broiler and turkey flocks (van Empel et al., 1997), indicates that the breeders of these flocks are in contact with O. rhinotracheale. Therefore, transmission by eggs may occur. The isolation of the organism from ovaries and oviducts of turkeys following experimental infection (Back et al., 1998b) supports the possibility of such vertical transmission. Varga et al. (2001) investigated the survival of O. rhinotracheale on eggshell and within chicken eggs during hatching. At 37°C, O. rhinotracheale did not survive on the eggshell for more than 24 hours, while upon inoculation into embryonated chicken eggs it killed embryos by the ninth day, and from the fourteenth day post-inoculation no O. rhinotracheale could be cultured. These results suggest that O. rhinotracheale is not transmitted via eggs during hatching.

Economic losses resulting from O. rhinotracheale infection are hard to estimate. The disease generally causes increased mortality, varying from 1% to higher than 10% (Hinz et al., 1994; van Beek et al., 1994; Hafez, 1996; Back et al., 1998b; Lombardi et al., 1999; Sakai et al., 2000) and growth retardation (van Beek et al., 1994; van Empel et al., 1996; van Veen et al., 2000a), which is difficult to determine. In layers, a significant drop in egg production has been reported (Joubert et al., 1999). Condemnation of carcasses due to airsacculitis in infected chickens and turkeys may cause additional economic losses (Back et al., 1998b). In the Netherlands, substantial financial losses have occurred due to high condemnation rates (up to 90%) of broilers at slaughter, with purulent airsacculitis as a prominent finding (van Veen et al., 2000a). A condemnation rate of 60% due to hydrops ascites, polyserositis and intra-abdominal concretions in broilers has been reported (van Veen et al., 2000a).

O. rhinotracheale has no known zoonotic significance (Chin and Droual, 1997).

There is no specific treatment for O. rhinotracheale infection. Therapeutic treatment of the disease can be difficult because acquired resistance against the regular antibiotics is very common (van Empel and Hafez, 1999). In suspected cases of O. rhinotracheale infection, identification of bacterial isolates and antimicrobial susceptibility testing is recommended. However, establishing the antibiotic sensitivity of O. rhinotracheale is difficult because of the organism’s complex growth requirements and the frequent occurrence of resistance (Devriese et al., 2001). Antibiotics have been used as part of an O. rhinotracheale treatment programme either singly or in a combination of oxytetracyclines in the water, chlortetracycline in the feed, or spectinomycin, ceftiofur, and penicillin by injection (Chin and Droual, 1997).

Devriese et al. (1995) investigated the antibiotic sensitivity of 14 strains of O. rhinotracheale from poultry and wild birds. They found that acquired antibiotic resistance is exceptionally frequent in isolates from poultry. Unlike the strains from wild birds, strains from gallinaceous birds had acquired resistance to penicillin-cephalosporin antibiotics and lincosamide and macrolide antibiotics. The resistance to beta-lactam antibiotics was relatively low. Acquired resistance was also frequently seen with quinolone and tetracycline antibiotics. Minimal inhibitory concentrations (MICs) of sulphamethoxazole-trimethoprim and spectinomycin were high, but no acquired resistance was evident. In a later study, Devriese et al. (2001) determined the minimal inhibitory concentrations of ten antibiotics (ampicillin, tylosin, lincomycin, doxycycline, ceftiofur, spiramycin, tilmicosin, flumequine, enrofloxacin and tiamulin) for 45 strains of O. rhinotracheale from Belgian broilers, collected between 1995 and 1998. They were compared with the type strain and a strain isolated from a rook. All the broiler strains were resistant to lincomycin and to the ß-lactams ampicillin and ceftiofur. Less than 10% of the strains were sensitive to the macrolides, tylosin and spiramycin, tilmicosin and flumequine. A few strains were sensitive to enrofloxacin and doxycycline while all strains were sensitive to tiamulin.

Fitzgerald et al. (1998) tested 25 O. rhinotracheale isolates for their susceptibility to fosfomycin (Fosbac). Ten of the isolates were susceptible to fosfomycin (MIC values <128 µg/ml) and all of these were able to agglutinate chicken red blood cells. The remaining 15 isolates were resistant to fosfomycin, with only five of these being able to agglutinate red blood cells, suggesting that there may be a correlation between susceptibility to fosfomycin and the ability to agglutinate red blood cells.

Varga et al. (2001) examined the antibiotic susceptibility of 12 O. rhinotracheale strains isolated from chickens and turkeys. Among the drugs examined, penicillin G, ampicillin (MICs ranging from =0.06 µg/ml to 1 µg/ml), ceftazidim (with MICs from =0.06 µg/ml to 0.12 µg/ml), erythromycin, tylosin, tilmicosin (with some exceptions MICs ranged from =0.06 µg/ml to 1 µg/ml) and tiamulin (MICs varied from =0.06 µg/ml to 2 µg/ml) were the most effective. Lincomycin, oxytetracycline and enrofloxacin also gave good inhibitions, but with most strains in a higher concentration (MICs ranged in most cases from 2 µg/ml to 8 µg/ml). The other antibiotics inhibited the growth of O. rhinotracheale only in a very high concentration (colistin) or not at all (apramycin, spectinomycin, polymyxin B).

Cefquinome and tilmicosin exhibited good in vitro antibacterial activity against O. rhinotracheale strains of poultry origin. The minimum inhibitory concentrations were 1.562 µg/ml and 0.78 µg/ml, respectively (Ak et al., 2001).