Bordetella Avium
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''Bordetella avium'' is a
gram negative The gram (originally gramme; SI unit symbol g) is a unit of mass in the International System of Units (SI) equal to one one thousandth of a kilogram. Originally defined as of 1795 as "the absolute weight of a volume of pure water equal to th ...
, nonfermentative, strictly
aerobic Aerobic means "requiring air," in which "air" usually means oxygen. Aerobic may also refer to * Aerobic exercise, prolonged exercise of moderate intensity * Aerobics, a form of aerobic exercise * Aerobic respiration, the aerobic process of cellu ...
,
motile Motility is the ability of an organism to move independently, using metabolic energy. Definitions Motility, the ability of an organism to move independently, using metabolic energy, can be contrasted with sessility, the state of organisms th ...
bacterium Bacteria (; singular: bacterium) are ubiquitous, mostly free-living organisms often consisting of one biological cell. They constitute a large domain of prokaryotic microorganisms. Typically a few micrometres in length, bacteria were among ...
from the genus ''
Bordetella ''Bordetella'' () is a genus of small (0.2 – 0.7 µm), gram-negative coccobacilli of the phylum Pseudomonadota. ''Bordetella'' species, with the exception of '' B. petrii'', are obligate aerobes, as well as highly fastidious, or difficult ...
'' which has been isolated from patients with respiratory disease (
cystic fibrosis Cystic fibrosis (CF) is a rare genetic disorder that affects mostly the lungs, but also the pancreas, liver, kidneys, and intestine. Long-term issues include difficulty breathing and coughing up mucus as a result of frequent lung infections. O ...
). ''B. avium'' has a global distribution, that mainly affects young domesticated turkeys. The disease in birds is called bordetellosis, and is largely associated with confined spaces and multi-aged flocks where management practices are sub optimal. In most infections,
mortality Mortality is the state of being mortal, or susceptible to death; the opposite of immortality. Mortality may also refer to: * Fish mortality, a parameter used in fisheries population dynamics to account for the loss of fish in a fish stock throug ...
is typically low but morbidity is very high. The
pathogenesis Pathogenesis is the process by which a disease or disorder develops. It can include factors which contribute not only to the onset of the disease or disorder, but also to its progression and maintenance. The word comes from Greek πάθος ''pat ...
of ''B. avium'' is through fimbrial attachment to the respiratory epithelium and release of a variety of
virulence Virulence is a pathogen's or microorganism's ability to cause damage to a host. In most, especially in animal systems, virulence refers to the degree of damage caused by a microbe to its host. The pathogenicity of an organism—its ability to ca ...
factors, leading to respiratory symptoms, such as sneezing, ocular and nasal discharge, and inflammation. Further complications include
edema Edema, also spelled oedema, and also known as fluid retention, dropsy, hydropsy and swelling, is the build-up of fluid in the body's Tissue (biology), tissue. Most commonly, the legs or arms are affected. Symptoms may include skin which feels t ...
, tracheal collapse, and decreased growth rate. Bordetellosis has a major impact on turkey health within turkey production systems but the impact in wild birds is not yet well defined. Good management practice and
biosecurity Biosecurity refers to measures aimed at preventing the introduction and/or spread of harmful organisms (e.g. viruses, bacteria, etc.) to animals and plants in order to minimize the risk of transmission of infectious disease. In agriculture, thes ...
protocols are essential for controlling disease caused by ''B. avium'' as the efficacy of antibiotics treatments for disease are variable, and prevention with
vaccination Vaccination is the administration of a vaccine to help the immune system develop immunity from a disease. Vaccines contain a microorganism or virus in a weakened, live or killed state, or proteins or toxins from the organism. In stimulating ...
s may not provide complete protection.


Microbial Characteristics

''Bordetella'' ''avium'' like other
Bordetella ''Bordetella'' () is a genus of small (0.2 – 0.7 µm), gram-negative coccobacilli of the phylum Pseudomonadota. ''Bordetella'' species, with the exception of '' B. petrii'', are obligate aerobes, as well as highly fastidious, or difficult ...
e is a
gram negative The gram (originally gramme; SI unit symbol g) is a unit of mass in the International System of Units (SI) equal to one one thousandth of a kilogram. Originally defined as of 1795 as "the absolute weight of a volume of pure water equal to th ...
coccobacillus. This
genus Genus ( plural genera ) is a taxonomic rank used in the biological classification of extant taxon, living and fossil organisms as well as Virus classification#ICTV classification, viruses. In the hierarchy of biological classification, genus com ...
is characterized by small aerobic bacteria (with the exception of B. ''petrii'' which is an anaerobe) that are
oxidase In biochemistry, an oxidase is an enzyme that catalyzes oxidation-reduction reactions, especially one involving dioxygen (O2) as the electron acceptor. In reactions involving donation of a hydrogen atom, oxygen is reduced to water (H2O) or hydro ...
and
catalase Catalase is a common enzyme found in nearly all living organisms exposed to oxygen (such as bacteria, plants, and animals) which catalyzes the decomposition of hydrogen peroxide to water and oxygen. It is a very important enzyme in protecting t ...
positive and nitrate reduction and
urease Ureases (), functionally, belong to the superfamily of amidohydrolases and phosphotriesterases. Ureases are found in numerous bacteria, fungi, algae, plants, and some invertebrates, as well as in soils, as a soil enzyme. They are nickel-containin ...
negative.Harrington A., Castelanos J., Ziedalski T., Clarridge J., and Cookson B. Isolation of Bordetella avium and Novel Bordetella Strain from Patients with Respiratory Disease. Emerg Infect Dis. 2009 Jan; 15(1): 72–74. doi: 10.3201/eid1501.071677 Bordetellae species produce two conserved toxins with a variety of additional toxins, individual to each species.Gentry-Weeks, C., Keith, J. M., & Thompson, J. (1993). Toxicity of Bordetella auium @-Cystathionase toward MC3T3-E 1 Osteogenic Cells*. THE JOURNAL OF BIOLOGICAL CHEMISTRY (Vol. 268). Unlike other Bordetellae, B. ''avium'' is motile and can grow in a filamentous form when grown in nutrient rich broth. Pathogenic strains grow readily on a variety of media including chocolate and trypticase soy agar, but
MacConkey agar MacConkey agar is a selective and differential culture medium for bacteria. It is designed to selectively isolate Gram-negative and enteric (normally found in the intestinal tract) bacteria and differentiate them based on lactose fermentation. ...
is recommended to differentiate this non fermentative bacterium from other fermentative species. Whereas passage attenuated colonies typically have a roughened surface; Pathogenic B. ''avium'' produces pearlescent colonies of 200-1000μm in diameter. When grown on MacConkey agar, pathogenic isolates often develop a darkened raised center.


Epidemiology

Turkey farming is a large industry with nearly 165 million kilograms of turkey products produced in Canada alone in 2019 ''.'' In the Turkey Health Survey released annually by the United States Animal Health Association ''B. avium'' has ranked between 5th and 8th over the past 5 years making it a remarkable issue for production health management ''.'' ''Bordetella avium'' has a worldwide distribution but is found at the highest density in the
North Temperate Zone In geography, the temperate climates of Earth occur in the middle latitudes (23.5° to 66.5° N/S of Equator), which span between the tropics and the polar regions of Earth. These zones generally have wider temperature ranges throughout t ...
, between the arctic circle and the Tropic of Cancer where the climate is most conducive to transfer. Seasonality of outbreaks are most often recorded during the summer and fall months. Outbreaks have been recorded in many countries including the United States, Canada, Australia, Germany, France, and South Africa. When infections do occur nearly all of the flock becomes affected leading to a high reported morbidity with low mortality. Severity of disease can be exacerbated by adverse environmental conditions (low temperature, high ammonia and dust, low humidity) and secondary bacterial infections; increasing mortality up to 40% or 60%. It is uncommon to see outbreaks in breeder flocks, but up to 20% morbidity with no mortality is reported. Furthermore, the bacterium is highly contagious and transmissible and the prevalence in bird species is abundant. Small backyard turkey flocks a mile from large commercial farms have shown isolated infections of ''B. avium.'' B. avium is not able to transmit via vertical transmission, but it can transmit by direct contact between birds and remain in the environment in litter, food, and water for as long as 6 months.''B. avium'' also has a short incubation of only 7–10 days allowing for easy and rapid transmission. Although birds of all ages are susceptible, prevalence is highest and most well understood in domesticated turkeys, especially in the younger populations consisting of birds 1–6 weeks old. It is thought that birds who reach 5–6 weeks of age become relatively resistant to the clinical disease bordetellosis, yet, they can remain carriers among the flock. In addition, much of the transmission is thought to relate to management practices and outbreaks are often associated with farms having confined spaces and flocks consisting of animals of varying ages. It is recommend that to limit disease transmission turkey farmers avoid multi-age flocks. Although less common, ''B. avium'' can also transmit to chickens as an
opportunistic infection An opportunistic infection is an infection caused by pathogens (bacteria, fungi, parasites or viruses) that take advantage of an opportunity not normally available. These opportunities can stem from a variety of sources, such as a weakened immune ...
, and wildlife species where prevalence is still being evaluated. It has been suggested that wildlife species act mainly as a reservoir and it is unclear if ''B. avium'' acts as part of the normal flora in wild bird populations or is a causative agent of disease. Despite the fact that wild birds are commonly asymptomatic, Bordetellosis has been reported in a variety of wild birds including parrot finches,
partridge A partridge is a medium-sized Galliformes, galliform bird in any of several genera, with a wide Indigenous (ecology), native distribution throughout parts of Europe, Asia and Africa. Several species have been introduced to the Americas. They a ...
s,
cockatiel The cockatiel (; ''Nymphicus hollandicus''), also known as weiro (also spelt weero), or quarrion, is a medium-sized parrot that is a member of its own branch of the cockatoo family endemic to Australia. They are prized as household pets and comp ...
s, and
ostrich Ostriches are large flightless birds of the genus ''Struthio'' in the order Struthioniformes, part of the infra-class Palaeognathae, a diverse group of flightless birds also known as ratites that includes the emus, rheas, and kiwis. There are ...
es, among others. In a study by Raffel ''et.al'', in a sample of 46
Canada geese The Canada goose (''Branta canadensis''), or Canadian goose, is a large wild goose with a black head and neck, white cheeks, white under its chin, and a brown body. It is native to the arctic and temperate regions of North America, and it is o ...
, 67% tested positive for ''B. avium'' using a serum agglutination test for antibodies. Beyond what is discussed here, many other studies have begun to look at characterizing the epidemiology of this bacterium. There is a strong interest in understanding the prevalence in different countries and prevalence among different species of domestic and wild birds. Understanding the epidemiology of this bacterium is of great importance to turkey producers as it remains one of the top 10 issues in domesticated turkeys. Unfortunately, as research stands, the full epidemiological understanding of this bacterium remains to be fully understood.


Virulence Factors

''B. avium'' exhibits its pathogenesis by attaching to the
cilia The cilium, plural cilia (), is a membrane-bound organelle found on most types of eukaryotic cell, and certain microorganisms known as ciliates. Cilia are absent in bacteria and archaea. The cilium has the shape of a slender threadlike projecti ...
on the respiratory epithelium of its host where it releases a number of
cytotoxins Cytotoxicity is the quality of being toxic to cells. Examples of toxic agents are an immune cell or some types of venom, e.g. from the puff adder (''Bitis arietans'') or brown recluse spider (''Loxosceles reclusa''). Cell physiology Treating cell ...
capable of causing damage to the tracheal cartilage and associated structures. Components enabling its attachment include
pili Pili may refer to: Common names of plants * ''Canarium ovatum'', a Philippine tree that is a source of the pili nut * ''Heteropogon contortus'', a Hawaiian grass used to thatch structures Places * Pili, Camarines Sur, is a municipality in the ...
, filamentous
hemagglutinin In molecular biology, hemagglutinins (or ''haemagglutinin'' in British English) (from the Greek , 'blood' + Latin , 'glue') are receptor-binding membrane fusion glycoproteins produced by viruses in the ''Paramyxoviridae'' family. Hemagglutinins ar ...
, fimbriae, protein autotransporters, outer membrane proteins such as
pertactin In molecular biology, pertactin (PRN) is a highly immunogenic virulence factor of ''Bordetella pertussis'', the bacterium that causes pertussis. Specifically, it is an outer membrane protein that promotes adhesion to tracheal epithelial cells. ...
, and other
lipopolysaccharide Lipopolysaccharides (LPS) are large molecules consisting of a lipid and a polysaccharide that are bacterial toxins. They are composed of an O-antigen, an outer core, and an inner core all joined by a covalent bond, and are found in the outer m ...
structures. The genes encoding for many of these proteins, such as ''fhaB'' (filamentous hemagglutinin) and ''fimA'' (fimbriae), as well as genes responsible for regulating the expression of virulence factors, such as ''bvgA'' (Bordetella virulence gene), have been identified and detected on confirmed isolates of ''B. avium.'' Identified cytotoxins produced by ''B. avium'' include an osteotoxin, a tracheal cytotoxin, a non-proteolytic dermonecrotic toxin that has been associated with nasal turbinate atrophy in pigs, and adenylate cyclase hemolysin with antiphagocytic activity. The osteotoxin is known to be cytotoxic for osteogenic cells and rat osteosarcoma cells, in addition to embryonic tracheal cells and fetal bovine trabecular cells. Its cytotoxic effect is achieved through the cleavage of L-cystine to form reactive sulfane-containing metabolites, which are then attached to proteins that are critical for the cell's survival. Virulence also requires iron, which is acquired through the use of heme receptors, siderophore receptors, and transferrin-binding proteins.


Clinical Significance

The typical host for ''Bordetella avium'' is the turkey. In turkeys this bacteria primarily leads to inflammation of the respiratory mucosa; clinically this can present as sneezing, altered breathing, lower growth rate, vocalization changes, clear discharge from the eyes and nose, tracheal collapse, and submandibular edema. These clinical signs are typically evident within 7–10 days after infection. In addition, their behaviour may change such that they are less active and will search out heat sources. On
necropsy An autopsy (post-mortem examination, obduction, necropsy, or autopsia cadaverum) is a surgical procedure that consists of a thorough examination of a corpse by dissection to determine the cause, mode, and manner of death or to evaluate any di ...
turkeys commonly have softened tracheal rings, mucous in the trachea and sinuses dorsal to the tracheal bifurcation, and hemorrhage present on the tracheal lining. B. avium has also been isolated from other wild and domesticated birds including chickens, mallards, Canada geese, cockatiels, and ostriches. It is uncertain if this bacterium causes disease in all these birds or if it is a part of their normal microbial flora. Chickens have been shown to be affected, however, they are not as severely affected with Bordetellosis as turkeys are. Most often this disease presents as severe respiratory disease in
broiler A broiler is any chicken (''Gallus gallus domesticus'') that is bred and raised specifically for meat production. Most commercial broilers reach slaughter weight between four and six weeks of age, although slower growing breeds reach slaughte ...
s, especially when they are concurrently infected with other respiratory viruses. Cockatiels and ostriches also have been shown to develop the disease but it has not yet been studied to determine how the disease presents in these birds. As the severity of disease increases the most common comorbidity associated with ''Bordetella avium'' is a secondary infection with ''E. coli.'' ''B. avium'' is also thought to decrease an individual's ability to clear secondary organisms from the trachea which allows them to set up an infection.
Zoonosis A zoonosis (; plural zoonoses) or zoonotic disease is an infectious disease of humans caused by a pathogen (an infectious agent, such as a bacterium, virus, parasite or prion) that has jumped from a non-human (usually a vertebrate) to a human. ...
''B. avium'' is an
opportunistic pathogen An opportunistic infection is an infection caused by pathogens (bacteria, fungi, parasites or viruses) that take advantage of an opportunity not normally available. These opportunities can stem from a variety of sources, such as a weakened immune ...
in humans and can cause respiratory disease, such as pneumonia, in immunocompromised patients. ''B. avium'' has also been isolated from human patients with
cystic fibrosis Cystic fibrosis (CF) is a rare genetic disorder that affects mostly the lungs, but also the pancreas, liver, kidneys, and intestine. Long-term issues include difficulty breathing and coughing up mucus as a result of frequent lung infections. O ...
(CF), however it is currently unclear if this bacteria is involved in the disease process of CF.Spilker, T.; Liwienski, A.A.; LiPuma, J.J. (2008-05). "Identification of Bordetella spp. in respiratory specimens from individuals with cystic fibrosis". ''Clinical Microbiology and Infection''. 14 (5): 504–506. doi:10.1111/j.1469-0691.2008.01968.x.
ISSN An International Standard Serial Number (ISSN) is an eight-digit serial number used to uniquely identify a serial publication, such as a magazine. The ISSN is especially helpful in distinguishing between serials with the same title. ISSNs ...
 1198-743X.


Control and Treatment

Environmental contamination is an important route of infection for ''B. avium''. ''B. avium'' can survive in the environment less than 2 days at higher temperatures (40 °C), up to a month with low temperature (10 °C) and humidity (32-58%), and up to 6 months in feed, water and damp litter. Good bio-security protocols, thorough cleaning, and excellent husbandry practices are the best methods for controlling outbreaks. Optimal temperature, humidity, and control of ammonia and dust are critical to reduce ''B.avium'' growth in the environment and reduce irritants to the tracheal epithelium. Most common disinfectants used do kill ''B. avium,'' and thorough cleaning includes removal of litter and other
fomite A fomite () or fomes () is any inanimate object that, when contaminated with or exposed to infectious agents (such as pathogenic bacteria, viruses or fungi), can transfer disease to a new host. Transfer of pathogens by fomites A fomite is any ina ...
s between flocks, disinfection of the barn and flushing of water lines with disinfectants, and
fumigation Fumigation is a method of pest control or the removal of harmful micro-organisms by completely filling an area with gaseous pesticides—or fumigants—to suffocate or poison the pests within. It is used to control pests in buildings (s ...
with methyl-bromide or
formaldehyde Formaldehyde ( , ) (systematic name methanal) is a naturally occurring organic compound with the formula and structure . The pure compound is a pungent, colourless gas that polymerises spontaneously into paraformaldehyde (refer to section F ...
. Foot baths, using on farm-clothing, controlling traffic between barns, preventing contact with wild birds, and showers between sites also reduces transmission between farms. For infected flocks, increasing ventilation and reaching optimal temperature are key. It has been reported that
niacin Niacin, also known as nicotinic acid, is an organic compound and a form of vitamin B3, an essential human nutrient. It can be manufactured by plants and animals from the amino acid tryptophan. Niacin is obtained in the diet from a variet ...
or 0.016% oxy-halogen added to water lines given early in life reduces the severity of bordetellosis. Antibiotic treatment is not considered effective for ''B. avium'' infections, as there is conflicting evidence for susceptibility; and most turkey poults with ''B.avium'' infection without secondary complications will recover from bordetellosis in 4–6 weeks, with resistance formed at 5–6 weeks. The mechanism of bacterial resistance in some strains of ''B. avium'' have been recorded: there are resistance genes encoded on
plasmid A plasmid is a small, extrachromosomal DNA molecule within a cell that is physically separated from chromosomal DNA and can replicate independently. They are most commonly found as small circular, double-stranded DNA molecules in bacteria; how ...
s (pRAM resistance genes to tetracycline and 2 sulfonamides) and lack of a penicillin binding protein 3 (PBP3) which drugs bind to, to inhibit cell wall synthesis. Plasmid conjugation between ''B. avium'' isolates also occurs. Most isolate strains of ''B. avium'' have resistance to a number of antibiotics. Resistance has been elucidated to aztreonam, ampicillin, tetracycline, cephalosporins, penicillins, sulbactam, sulfonamides, streptomycin, carbapenem, imipenem, fluoroquinolones, chloramphenicol, gentamicin, cefoperazone, cefepime, ceftazidime, piperacillin and amikacin.  However, some susceptibility has also been shown to ampicillin, amoxicillin, penicillin, ceftiofur, enrofloxacin, norfloxacin, ciprofloxacin, erythromycin, florfenicol, and co-trimoxazole. The difficulty with characterizing antibiotic resistance and susceptibility in ''B. avium'' strains is most strains will appear sensitive ''
in vitro ''In vitro'' (meaning in glass, or ''in the glass'') studies are performed with microorganisms, cells, or biological molecules outside their normal biological context. Colloquially called "test-tube experiments", these studies in biology an ...
,'' but in reality has a much different outcome ''
in vivo Studies that are ''in vivo'' (Latin for "within the living"; often not italicized in English) are those in which the effects of various biological entities are tested on whole, living organisms or cells, usually animals, including humans, and ...
''. Isolates are believed to be sensitive ''in vitro'' but not ''in vivo'' due to the inability of the drug to reach therapeutic doses within the tracheal epithelium of turkeys where bacteria dwell. Two vaccines are available for poultry against ''B''. ''avium'' bordetellosis: a temperature sensitive mutant live strain of ''B.avium'' and a bacterin isolate vaccine. Bacterins are administered to breeder hens to induce maternal
IgG Immunoglobulin G (Ig G) is a type of antibody. Representing approximately 75% of serum antibodies in humans, IgG is the most common type of antibody found in blood circulation. IgG molecules are created and released by plasma B cells. Each IgG ...
to pass onto their progeny, providing maternal immunity up to 4 weeks in poults. The mutant live-strain is administered to poults twice; at hatchery and then at 2–3 weeks of age. However, vaccines are not known to be very efficacious, and may only protect against severe clinical signs, or delay onset of disease, not stop the spread of infection. Most significant immunity in turkey poults is thought to be acquired humoral immunity at this time. Vaccinations are considered for prevention if there is recurrence in outbreaks of bordetellosis.


References


External links


Type strain of ''Bordetella avium'' at Bac''Dive'' - the Bacterial Diversity Metadatabase
{{DEFAULTSORT:Bordetella avium Burkholderiales Bacteria described in 1984