Invasive Species Compendium

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Mannheimia haemolytica

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Datasheet

Mannheimia haemolytica

Summary

  • Last modified
  • 22 January 2019
  • Datasheet Type(s)
  • Invasive Species
  • Preferred Scientific Name
  • Mannheimia haemolytica
  • Taxonomic Tree
  • Domain: Bacteria
  •   Phylum: Proteobacteria
  •     Class: Gammaproteobacteria
  •       Order: Pasteurellales
  •         Family: Pasteurellaceae
  • Summary of Invasiveness
  • Mannheimia haemolytica is a Gram-negative corresponding to Pasteurella haemolytica biogroup 1 which in 1999 was renamed as Mannheimia. It is an important cause of bacterial respiratory mortali...

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Pictures

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PictureTitleCaptionCopyright
M. haemolytica on blood agar plate; haemolysis is not evident.
TitleBlood agar plate
CaptionM. haemolytica on blood agar plate; haemolysis is not evident.
CopyrightPiera Anna Martino
M. haemolytica on blood agar plate; haemolysis is not evident.
Blood agar plateM. haemolytica on blood agar plate; haemolysis is not evident.Piera Anna Martino
Electron-microscope image.
TitleEM
CaptionElectron-microscope image.
CopyrightPiera Anna Martino
Electron-microscope image.
EMElectron-microscope image.Piera Anna Martino

Identity

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Preferred Scientific Name

  • Mannheimia haemolytica

Other Scientific Names

  • Bacillus bovisepticus
  • Pasteurella haemolytica
  • Pasteurella mastitides

Summary of Invasiveness

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Mannheimia haemolytica is a Gram-negative corresponding to Pasteurella haemolytica biogroup 1 which in 1999 was renamed as Mannheimia. It is an important cause of bacterial respiratory mortality in cattle, sheep and goats, in particular causing the economically significant cattle disease known as bovine pneumonic pasteurellosis or mannheimiosis, or shipping fever. It is also responsible for mastitis in ewes and camels, and rarely for abortion in cattle. It also causes a rare respiratory disease in pigs associated with Actinobacillus pleuropneumoniae, and it has been isolated from some wild and domesticated birds. Although it is not normally an important zoonotic agent, it can cause serious disease in human infants and immunocompromised adults, and it has been demonstrated in septicaemia of infants and in adults with heart disease.

Healthy animals carry M. haemolytica as a nasal and nasopharyngeal commensal without developing clinical signs. However, when cattle (particularly younger animals) are stressed (for example in transportation from pastured herds to feedlots), and/or become infected with respiratory viruses, M. haemolytica replicates and is inhaled into the lower respiratory tract where it causes great damage. Other opportunistic bacteria such as Pasteurella multocida, Histophilus somni, or Trueperella pyogenes (formerly Arcanobacterium pyogenes) can also take advantage of the damage done to the respiratory tissue. The interaction between the various pathogens can cause respiratory disease, which as a result is often referred to as bovine respiratory disease complex.

Infection is treated with antibiotics, and vaccines are used to try to prevent it.

M. haemolytica is already found worldwide where suitable hosts are present. Its origins are unclear, in particular because until recently it was not distinguished from Pasteurella multocida.

Taxonomic Tree

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  • Domain: Bacteria
  •     Phylum: Proteobacteria
  •         Class: Gammaproteobacteria
  •             Order: Pasteurellales
  •                 Family: Pasteurellaceae
  •                     Genus: Mannheimia
  •                         Species: Mannheimia haemolytica

Notes on Taxonomy and Nomenclature

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M. haemolytica (from Greek haima - blood, lyt – adverb form of verb lyo - dissolve, and adjectival suffix – ikos latinized in – ica) was formerly classified as Pasteurella haemolytica biogroup 1, and there were two P. haemolytica biotypes, A and T for arabinose or trehalose fermentation (Bisgaard and Mutters, 1986). Seventeen serotypes were described for P. haemolytica. Biotype T strains, i.e. serotypes 3, 4, 10, 11, 15 and 17, were reclassified as Pasteurella trehalosi and later as Bibersteinia trehalosi (Blackall et al., 2007; Sneath and Stevens, 1990). The biotype A strains, i.e. serotypes 1, 2, 5, 6, 7, 8, 9, 12, 13, 14 and 16, were reclassified as M. haemolytica (Angen et al., 1999a; Angen et al., 1999b), which is the subject of this datasheet. The name Mannheimia is a tribute to Walter Mannheim, a German microbiologist who studied the taxonomy of the family Pasteurellaceae (Angen et al., 1999a; Angen et al., 1999b).

Distribution

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The geographical distribution of Mannheimia haemolytica is worldwide, although specific references for every country were not available for the Distribution table. The microorganism is reported most frequently in Asia and in countries where sheep or goat breeding is widespread, such as in Africa and North America. In Europe, pasteurellosis or mannheimiosis is also widespread and involves many countries where sheep and cattle are present, such as the Netherlands, Denmark, Germany, Italy and France (Topolko and Benic, 1997; Tefera and Smola, 2002a,b; Angen et al., 2002; Thomas et al., 2001; Ewers et al., 2004Fels-Klerx et al., 2002; Catana et al., 1997; Lyakh and Androsik, 1996; Harwood, 2004).

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

IndiaPresentRajesh et al., 2000
-Himachal PradeshPresentRajesh et al., 2000
-RajasthanPresentMishra et al., 2000
IranPresentSasani et al., 2002
IraqPresentAl-Sultan, 1995
IsraelPresentYeruham et al., 1999
JapanPresentNakaya et al., 1998; Katsuda et al., 2003
JordanPresentAl-Tarazi, 2002
Korea, Republic ofPresentKang et al., 2001
MalaysiaPresentSabri et al., 2013; Chung et al., 2015
PakistanReported present or known to be presentNativeKhan and Khan, 1997
Saudi ArabiaPresentIsmail and Hatem, 1998
Sri LankaPresentJayaweera et al., 2014
SyriaPresentKasouha et al., 2009
TurkeyPresentYener et al., 2001
VietnamPresentLe and Pham, 1998

Africa

BeninPresentAdehan et al., 2006
CameroonPresentMartrenchar et al., 1995
EgyptPresentSeddek, 2002; Ali and Youssef, 2003
EthiopiaPresentWoubit et al., 2001; Sisay and Zerihun, 2003
NigeriaPresentOdugbo et al., 2004; Ekong et al., 2014
South AfricaPresentOdendaal and Henton, 1995
SudanPresentElsheikh and Hassan, 2012
ZimbabwePresentDziva and Mohan, 2000

North America

CanadaPresentBooker et al., 1999
-AlbertaPresentMartin et al., 1998
-ManitobaPresentWard et al., 1999
-OntarioPresentO'Connor et al., 2001
MexicoPresentPijoan and Chavez, 2003
USAReported present or known to be presentNativeFrank, 1998; Singer et al., 1998
-CaliforniaPresentSinger et al., 1998
-ColoradoPresentStevens et al., 1997
-IdahoPresentMiller et al., 2012
-IowaPresentAl-Ghamdi et al., 2000
-KansasPresentWard et al., 1999
-MichiganPresentAl-Ghamdi et al., 2000
-MinnesotaPresentWard et al., 1999
-MontanaPresentWard et al., 1999
-NebraskaPresentHarhay et al., 2013
-NevadaPresentWard et al., 1999
-New MexicoPresentFrank et al., 2002
-North DakotaPresentWard et al., 1999
-OklahomaPresentTaylor et al., 2015
-OregonPresentMiller et al., 2012
-South DakotaPresentDaniel et al., 2006
-TennesseePresentFrank et al., 2002
-TexasPresentPurdy et al., 2001
-WyomingPresentMiller et al., 2012

South America

ArgentinaPresentAuad et al., 2001
BrazilLocalisedPresent based on regional distribution
-Minas GeraisPresentAraujo et al., 2009
-ParaibaPresentSilva et al., 2009
-Rio Grande do SulPresentFarias et al., 2013
PeruPresentRosadio et al., 2011

Europe

BelgiumPresentCatry et al., 2002
CroatiaPresentTopolko and Benic, 1997
Czech RepublicPresentTefera and Smola, 2002a
DenmarkPresentAngen et al., 2002
FrancePresentThomas et al., 2001
GermanyPresentEwers et al., 2004
GreecePresentFthenakis, 1994
HungaryPresentMiklós et al., 1999
ItalyPresentZizzo et al., 2003
NetherlandsPresentFels-Klerx et al., 2002
NorwayPresentStuen et al., 2007
RomaniaPresentCatana et al., 1997
Russian FederationPresentLyakh and Androsik, 1996
SpainPresentRedondo et al., 1994
SwedenPresentSchwan, 1998
UKPresentHarwood et al., 1995

Oceania

AustraliaPresentBlackall et al., 2002
-New South WalesPresentTaylor, 1998
-QueenslandPresentTaylor, 1998
New ZealandPresentAlley, 2002

History of Introduction and Spread

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M. haemolytica has likely been a commensal within the respiratory tract of cattle for decades. Originally called Bacillus bovisepticus, it was recognized as a pathogen in bovine pneumonia in the early 20th century (Hepburn, 1925; Jones, 1921). Much of the early understanding of the bacterium in respiratory disease is clouded by it not being readily separated from Pasteurella multocida infections.

Pathogen Characteristics

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(This section includes information from Confer (2009)).

Mannheimia haemolytica is a Gram-negative, non-motile, small rod- and coccobacillus-shaped bacterium. It is often bipolar stained (‘safety pin’) with Gram’s stain. Colonies are smooth and greyish on blood agar and are 1-2 mm in width after 24 h of incubation. Most strains show a characteristic faint β-haemolysis on bovine blood agar. Biochemical reactions are several: D-sorbitol, D-xylose, maltose and dextrin are fermented, while no strains ferment L-arabinose or glucosides. Strains are negative for ornithine decarboxylase and β-glucosidase and positive for α-fucosidase (Angen et al., 1999a).

M. haemolytica was formerly classified as Pasteurella haemolytica biogroup 1, and there were two P. haemolytica biotypes, A and T for arabinose or trehalose fermentation (Bisgaard and Mutters, 1986). Seventeen serotypes were described for P. haemolytica. Biotype T strains were reclassified as Pasteurella trehalosi and later as Bibersteinia trehalosi (Blackall et al., 2007; Sneath and Stevens, 1990). The bacterium M. haemolytica is composed of serotypes 1, 2, 5, 6, 7, 8, 9, 12, 13, 14 and 16 (Angen et al., 1999a; Angen et al., 1999b). The G and C content of the DNA of the type strain is 43.6 molar percentage.

M. haemolytica is part of the normal nasopharyngeal flora in cattle, sheep and goats, and when the animal is stressed or suffers from a viral infection, the bacterium proliferates and is inhaled into the lungs where it can cause severe pneumonia (Rice et al., 2007). Although most of the cases of pneumonia arise from the M. haemolytica strain that is carried by the particular bovine, molecular evidence indicates that there is a certain amount of horizontal transmission from animal to animal during an outbreak of pneumonia (Timsit et al., 2013).

There are many pathogenicity (virulence) factors of M. haemolytica: fimbriae, capsule, lipopolysaccharide (LPS), proteins and lipoproteins of the outer membrane, systems of iron uptake, leukotoxin and extracellular enzymes (Confer, 2009). Each pathogenicity factor is described in detail below.

Capsule

M. haemolytica is encapsulated during the logarithmic growth phase. The capsule is composed of disaccharide repeats of N-acetylmannosaminuronic acid β-1,4 linked with N-acetylmannosamine (McKerral and Lo, 2002). Encapsulation enhances bacterial resistance to phagocytosis and complement mediated killing and functions as an adhesin in the lung (Chae et al., 1990).  The capsular polysaccharide is immunogenic; however, antibody responses to capsular polysaccharide do not correlate with resistance against experimental challenge (Confer, 2009).

Fimbriae

At least two types of fimbriae have been demonstrated, in vitro, on serotype 1, namely a rigid 12 nm-wide structure and a flexible 5 nm-wide fimbria (Morck et al., 1987; Potter et al., 1988). In vivo, strains isolated from broncho-alveolar lavage or adherent to the tracheal epithelium have structures that resemble fimbriae. Their role is not completely known, but they are likely to be one of the adhesins responsible for adhesion of the bacteria to the respiratory epithelium.

Lipopolysaccharide

As in other Gram-negative bacteria, the cell wall of M. haemolytica contains lipopolysaccharide (LPS); the lipid A component is responsible for endotoxin-induced local and systemic pathologic processes. There are variations in LPS profiles among and within serotypes.  For instance, serotype 1 isolates are often smooth  type LPS, whereas serotype 2 isolates are usually rough types (McCluskey et al., 1994). The intravenous injection of purified LPS in calves causes release of thromboxane A2, prostaglandins, serotonin, cyclic adenosine monophosphate (cAMP) and cyclic guanosine monophosphate (cGMP) (Rice et al., 2007). All or some of these mediators may be responsible for the clinical signs associated with endotoxic shock. If this situation arises, the antibodies directed against LPS of M. haemolytica do not correlate with resistance against experimental infection. Within the respiratory tract, LPS results in vascular damage through release of proinflammatory cytokines, activation of complement and coagulation cascade, and direct cytolysis (Singh et al., 2011).

Proteins and lipoproteins of outer membrane

Many proteins of the outer membrane, with a molecular weight (MW) of 28-40 kDa, can be chemotactic for neutrophils but reduce neutrophilic phagocytosis and lysis of the ingested bacteria (Iovane et al., 1998). Three tandem, membrane lipoproteins (MW=29-30 kDa) act by opposing activation of the complement cascade (Murphy et al., 1998). Two major proteins of the outer membrane, PomA and PomB, have been identified in strains belonging to serovar 1. PomA protein is similar to OmpA of Escherichia coli and has subsequently been referred to as M. haemolytica OmpA; it binds fibronectin and facilitates adhesion to bronchial epithelium (Confer and Ayalew, 2013; Kisiela and Czuprynski, 2009; Lo and Sorensen, 2007; Mahasreshti et al., 1997).

M. haemolytica  does not produce siderophores and utilizes a transferrin binding system of iron uptake (Rice et al., 2007). Two transferrin-binding outer membrane proteins are produced that specifically bind bovine transferrin, which allows the bacterium to extract and utilize iron from transferrin. The gene tbpA codes for the TbpA protein of 100 kDa and the tbpB gene codes for the TbpB protein of 71 kDa. In vivo, these proteins are immunogenic and are protective for experimentally infected specific pathogen free (SPF) sheep (Potter et al., 1999).

Leukotoxin 

M. haemolytica leukotoxin is one of a family of functionally and genetically similar bacterial toxins, all of which contain repeating domains in the toxin molecule and are designated RTX toxins (repeat domains in the structural toxin) (Lo et al., 1987; Rice et al., 2007). Bacteria that produce RTX toxins include Actinobacillus actinomycetemcomitans [Aggregatibacter actinomycetemcomitans], A. pleuropneumoniae, A. suis, A. equuli subspecies haemolyticus, Bordetella pertussis, hemolytic Escherichia coli strains, and others (Frey and Kuhnert, 2002). M. haemolytica leukotoxin has 6 repeat domains, which are rich in glycine and contain 9 amino acids. All M. haemolytica serotypes produce this soluble, heat-labile leukotoxin with exclusive specificity for leukocytes of ruminants by binding to CD11a/CD18 (Davies and Baillie, 2003; Larsen et al., 2009). Non-toxic isolates are rarely found. At low concentrations, this toxin impairs phagocytosis and lymphocyte proliferation; higher concentrations result in cell death due to lysis (Rice et al., 2007). Lysis results from formation of 0.9- to 1.2-mm transmembrane pores in the target cell, which allows the movement of potassium, sodium and calcium along transmembrane gradients (Clinkenbeard et al., 1989). The enzymes released following cytolysis and the leukotoxin itself are chemotactic for other leukocytes and augment lung damage due to increased cell recruitment in this area. In addition, leukotoxin is lytic for ruminant platelets, lysis of which may induce pulmonary vascular thrombosis and fibrin exudation, which is typical of shipping pneumonia (Clinkenbeard and Upton, 1991). The genes involved in leukotoxin production and secretion are designated lktA, lktB, lktC and lktD and are necessary for the production of active toxin. Gene products of lktB and lktD facilitate secretion of the toxin, and the product of lktC is involved with toxin activation (Highlander, 2001).

Extracellular enzymes

(Information from Rice et al., 2007)

At least 4 enzymes secreted by bacteria can facilitate colonization of pulmonary alveoli or reduce the effect of defensive mechanisms:

Sialoglycoprotease is a neutral protease, coded by the gcp gene and present in all the M. haemolytica strains; it specifically hydrolyses O-sialoglycoproteins associated with host cell membranes.

Neuraminidase, which hydrolyzes sialic acid from cell surface molecules, is produced by all the strains during the stationary phase of bacterial growth, and is also produced in vivo.

Superoxide dismutase, which catalyzes the conversion of superoxide radicals to hydrogen peroxide and oxygen, is produced only by serotypes 1 and 2

IgG1 protease, which cleaves bovine IgG1, thus reducing the efficacy of the immune response, was described in serotype 1. The enzyme is similar to or may in fact be the sialoglycoprotease, because sequence studies have failed to identify a specific gene for the enzyme.

Economic Impact

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In the USA, pneumonia caused by M. haemolytica is the main cause of economic losses in the breeding of calves. The same condition is also observed in Europe (Fels-Klerx et al., 2002). In addition, M. haemolytica is the second commonest agent causing mastitis in goats in Europe and is one of the main aetiological agents of this disease in USA. Gelasakis et al. (2015) report that sheep mastitis due to M. haemolytica and Staphylococcus aureus causes substantial economic and disease losses to the sheep industry

Financial losses that result from calf pneumonia occur due to death, treatment cost and decreased lifetime productivity (and possibly a lower grade of meat in cattle treated multiple times for the disease). Michigan dairy producers estimated that respiratory disease in calves cost them US $14.71 per calf/year (Kaneene and Hurd, 1990) while producers in California estimated that calf respiratory disease cost them US $9 per calf/year (Sischo et al., 1990). The economic loss is over US $1 billion in North American beef and dairy cattle (Miles, 2009) (Griffin, 1997).

A study in two dairies in Mexico (Pijoan and Chavez, 2003) evaluated direct and indirect costs of losses due to pneumonia. Direct costs included fatalities, discards and treatment. Indirect costs included vaccination and preventive treatment. The range varied from US $52.78 per calf to US $24.72 per calf.

Environmental Impact

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In free ranging North American Bighorn sheep (Ovis canadensis), M. haemolytica (and also Bibersteinia trehalosi) cause severe pneumonia in all age groups (Besser et al., 2013). These bacteria have been largely responsible for the large decline in the Bighorn sheep population.

Social Impact

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Because respiratory disease is the major cause of economic losses in the beef cattle industry and M. haemolytica is such a major cause of bovine pneumonia, antibiotics are used in large amounts to control the pneumonia (Rice et al., 2007).  This practice has led to concern that high antibiotic use in meat and dairy cattle can lead to antimicrobial resistance in human pathogens (Oliver et al., 2011).

Although M. haemolytica is not normally an important zoonotic agent, it can cause serious disease in human infants and immunocompromised adults; it has been demonstrated in septicaemia of infants and in adults with heart disease (Punpanich and Srijuntongsiri, 2012; Takeda et al., 2003).

Risk and Impact Factors

Top of page Invasiveness
  • Invasive in its native range
  • Proved invasive outside its native range
  • Abundant in its native range
  • Fast growing
  • Has high reproductive potential
  • Reproduces asexually
  • Has high genetic variability
Impact outcomes
  • Host damage
  • Negatively impacts agriculture
  • Negatively impacts animal health
  • Negatively impacts livelihoods
  • Threat to/ loss of endangered species
Impact mechanisms
  • Pathogenic
Likelihood of entry/control
  • Highly likely to be transported internationally accidentally
  • Difficult/costly to control

Gaps in Knowledge/Research Needs

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We lack understanding of the host and organism factors that allow M. haemolytica to out-compete other bacteria of the upper respiratory tract, thus allowing it to be inhaled into the lungs and cause disease. 

References

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Adehan, R. K., Ajuwape, A. T. P., Adetosoye, A. I., 2006. The occurrence Mycoplasma species and other bacteria in pneumonic lungs of sheep and goats. Folia Veterinaria, 50(2), 76-79.

Al-Ghamdi, G. M., Ames, T. R., Baker, J. C., Walker, R., Chase, C. C. L., Frank, G. H., Maheswaran, S. K., 2000. Serotyping of Mannheimia (Pasteurella) haemolytica isolates from the upper Midwest United States. Journal of Veterinary Diagnostic Investigation, 12(6), 576-578.

Ali, A. R., Youssef, A. E., 2003. Bacteriological studies and biochemical parameters of respiratory infection in ostriches. Veterinary Medical Journal Giza, 51(2), 189-203.

Alley, M. R., 2002. Pneumonia in sheep in New Zealand: an overview. New Zealand Veterinary Journal, 50(3 Supplement), 99-101.

Al-Sultan, I. I., 1995. Prevalence of Pasteurella haemolytica serotypes causing pneumonic pasteurellosis in Iraqi sheep. Iraqi Journal of Veterinary Sciences, 8(1), 163-166.

Al-Tarazi, Y. H. M., 2002. The efficacy of an experimental Pasteurella hemolytica vaccine as measured by seroconversion in Awassi lambs in Jordan. Small Ruminant Research, 45(2), 201-208. doi: 10.1016/S0921-4488(02)00101-3

Angen Ø, Mutters R, Caugant DA, Olsen JE, Bisgaard M, 1999. Taxonomic relationships of the [Pasteurella] haemolytica complex as evaluated by DNA-DNA hybridizations and 16S rRNA sequencing with proposal of Mannheimia haemolytica gen. nov., comb. nov., Mannheimia granulomatis comb. nov., Mannheimia glucosida sp. nov., Mannheimia ruminalis sp. nov. and Mannheimia varigena sp. nov. International Journal of Systematic Bacteriology, 49(1):67-86; 69 ref

Angen, Ø., Ahrens, P., Bisgaard, M., 2002. Phenotypic and genotypic characterization of Mannheimia (Pasteurella) haemolytica-like strains isolated from diseased animals in Denmark. Veterinary Microbiology, 84(1/2), 103-114. doi: 10.1016/S0378-1135(01)00439-4

Angen, Ø., Quirie, M., Donachie, W., Bisgaard, M., 1999. Investigations on the species specificity of Mannheimia (Pasteurella) haemolytica serotyping. Veterinary Microbiology, 65(4), 283-290. doi: 10.1016/S0378-1135(98)00304-6

Araujo, M. R. de, Costa, M. C., Ecco, R., 2009. Occurrence of pneumonia associated to infection by Mannheimia haemolytica in sheep of Minas Gerais. Pesquisa Veterinária Brasileira, 29(9), 719-724. http://www.scielo.br/pdf/pvb/v29n9/a07v29n9.pdf doi: 10.1590/S0100-736X2009000900007

Auad, J., Carbonero Martínez, A., Victoria Maure, M. V., Daffner, J. F., Gleser, H. D., 2001. Inoculation trial and humoral response with an inactivated oily vaccine against the bovine respiratory complex (BRC). Veterinaria Argentina, 18(176), 430-439.

Besser, T. E., Cassirer, E. F., Highland, M. A., Wolff, P., Justice-Allen, A., Mansfield, K., Davis, M. A., Foreyt, W., 2013. Bighorn sheep pneumonia: sorting out the cause of a polymicrobial disease. Preventive Veterinary Medicine, 108(2/3), 85-93. http://www.sciencedirect.com/science/journal/01675877 doi: 10.1016/j.prevetmed.2012.11.018

Bisgaard M, Mutters R, 1986. Re-investigations of selected bovine and ovine strains previously classified as Pasteurella haemolytica and description of some new taxa within the Pasteurella haemolytica-complex. Acta Pathologica, Microbiologica et Immunologica Scandinavica, B, 94(3):185-193; 27 ref

Blackall, P. J., Bisgaard, M., Stephens, C. P., 2002. Phenotypic characterization of Australian sheep and cattle isolates of Mannheimia haemolytica, Mannheimia granulomatis and Mannheimia varigena. Australian Veterinary Journal, 80(1/2), 87-91. doi: 10.1111/j.1751-0813.2002.tb12058.x

Blackall, P. J., Bojesen, A. M., Christensen, H., Bisgaard, M., 2007. Reclassification of [Pasteurella] trehalosi as Bibersteinia trehalosi gen. nov., comb. nov. International Journal of Systematic and Evolutionary Microbiology, 57(4), 666-674. http://ijs.sgmjournals.org doi: 10.1099/ijs.0.64521-0

Booker, C. W., Guichon, P. T., Jim, G. K., Schunicht, O. C., Harland, R. J., Morley, P. S., 1999. Seroepidemiology of undifferentiated fever in feedlot calves in western Canada. Canadian Veterinary Journal, 40(1), 40-48.

Catana, N., Necsulescu, M., Lazau, A., Herman, V., Ramneantu, M., Ciorba, D., 1997. The prevalence of Pasteurella infections in calves with respiratory diseases. (Prevalenta infectiei cu pasteurella la viteii cu afectiuni respiratorii). In: Al 22-lea simpozion, Cluj-Napoca, 1996. Actualita?i în patologia animalelor domestice: lucrari ?tiin?ifice . Cluj-Napoca, Romania: Universitatea de Stiinte Agricole, Cluj-Napoca. 288-290.

Catry, B., Govaere, J. L. J., Devriese, L., Laevens, H., Haesebrouck, F., Kruif, A. de, 2002. Bovine enzootic bronchopneumonia: prevalence of pathogens and its antimicrobial susceptibility. Vlaams Diergeneeskundig Tijdschrift, 71(5), 348-354.

Chae, C. H., Gentry, M. J., Confer, A. W., Anderson, G. A., 1990. Resistance to host immune defense mechanisms afforded by capsular material of Pasteurella haemolytica, serotype 1. Veterinary Microbiology, 25(2/3), 241-251. doi: 10.1016/0378-1135(90)90081-6

Chung LimTeik [Chung, L. T. E. ], Faez Firdaus, J. A., Abba, Y., Tijjani, A., Sadiq, M. A., Mohammed, K., Abdinasir Yusuf Osman, Adamu, L., Mohd Azmi, M. L., Abdul Wahid Haron, 2015. Clinical management of pneumonic pasteurellosis in Boer kids: a case report. International Journal of Livestock Research, 5(4), 100-104. http://www.scopemed.org/fulltextpdf.php?mno=183834

Clinkenbeard, K. D., Mosier, D. A., Confer, A. W., 1989. Transmembrane pore size and role of cell swelling in cytotoxicity caused by Pasteurella haemolytica leukotoxin. Infection and Immunity, 57(2), 420-425.

Clinkenbeard, K. D., Upton, M. L., 1991. Lysis of bovine platelets by Pasteurella haemolytica leukotoxin. American Journal of Veterinary Research, 52(3), 453-457.

Confer, A. W., 2009. Update on bacterial pathogenesis in BRD. Animal Health Research Reviews, 10(2), 145-148. http://journals.cambridge.org/action/displayAbstract?fromPage=online&aid=6865224&next=true&jid=AHR&volumeId=10&issueId=02 doi: 10.1017/S1466252309990193

Confer, A. W., Ayalew, S., 2013. The OmpA family of proteins: roles in bacterial pathogenesis and immunity. Veterinary Microbiology, 163(3/4), 207-222. http://www.sciencedirect.com/science/journal/03781135 doi: 10.1016/j.vetmic.2012.08.019

Daniel, J. A., Held, J. E., Brake, D. G., Wulf, D. M., Epperson, W. B., 2006. Evaluation of the prevalence and onset of lung lesions and their impact on growth of lambs. American Journal of Veterinary Research, 67(5), 890-894. doi: 10.2460/ajvr.67.5.890

Davies RL, Baillie S, 2003. Cytotoxic activity of Mannheimia haemolyitica strains in relation to diversity of the leukotoxin structural gene lktA. Veterinary Microbiology, 92:263-279

Dziva, F., Mohan, K., 2000. Pasteurellosis and Pasteurellae in Zimbabwe: an update. Zimbabwe Veterinary Journal, 31(1), 1-10.

Ekong, P. S., Akanbi, B. O., Odugbo, M. O., 2014. A case report of respiratory Mannheimiosis in sheep and goat complicated by Bordetella parapertussis. Nigerian Veterinary Journal, 35(2), 968-974. http://www.ajol.info/index.php/nvj/article/view/112582/102334

Elsheikh, H. M., Hassan, S. O., 2012. Pneumonia in goats in Sudan. International Journal of Animal and Veterinary Advances, 4(2), 144-145. http://maxwellsci.com/print/ijava/v4-144-145.pdf

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Pneumonic Pasteurellosis – Iowa State Universityhttps://vetmed.iastate.edu/vdpam/FSVD/swine/index-diseases/pneumonic-pasteurellosis

Contributors

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30/04/2017 Revised for Invasive Species Compendium by:

Anthony W. Confer, Oklahoma State University, Stillwater, Oklahoma, USA

30/11/2004 Original text by:

Piera Martino, University of Milan, Italy.

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