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Bibersteinia trehalosi infections

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Bibersteinia trehalosi infections

Summary

  • Last modified
  • 03 January 2018
  • Datasheet Type(s)
  • Animal Disease
  • Preferred Scientific Name
  • Bibersteinia trehalosi infections
  • Overview
  • Originally described as biotype T (trehalose fermenting) of the [Pasteurella] haemolytica complex, Bibersteinia trehalosi was recognized as a separate species (named Pasteurella trehalos...

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Identity

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Preferred Scientific Name

  • Bibersteinia trehalosi infections

Overview

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Originally described as biotype T (trehalose fermenting) of the [Pasteurella] haemolytica complex, Bibersteinia trehalosi was recognized as a separate species (named Pasteurella trehalosi) in 1990 (Sneath and Stevens, 1990). The organism was reclassified as Bibersteinia trehalosi in 2007 on the basis of phylogenetic studies (Blackall et al., 2007).

B. trehalosi is an important pathogen of sheep, primarily associated with septicaemia in older lambs (Gilmour, 1978; Sneath and Stevens, 1990; Donachie, 2007), and less commonly with respiratory disease (Miller et al., 2011; Gonzalez et al., 2013). B. trehalosi has also been isolated from bighorn sheep with pneumonia (Rudolph et al., 2007; Wolfe et al., 2010; Drew et al., 2014) and from goats with pasteurellosis (Sanchis and Abadie, 1992; Guillou, 2004; Abadie and Thiery, 2006).

B. trehalosi has been isolated from cases of bovine respiratory disease (Collins, 2011; Cortese et al., 2012) but its role as a primary pathogen in cattle is uncertain.

Hosts/Species Affected

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Bibersteinia trehalosi is a common inhabitant of the upper respiratory tracts and tonsils of healthy sheep (Al-Sultan and Aitken, 1985). B. trehalosi can cause ovine systemic pasteurellosis and/or septicaemia in feeding lambs, most commonly following a period of stress or management change (Sanchis et al., 1991; Sanchis and Abadie, 1992; Davies et al., 1997). Some B. trehalosi strains have also been found to be involved in wild ruminant pneumonia (Villard et al., 2006; Dassanayake et al., 2013).

B. trehalosi is considered normal flora in the tonsils of bison (Bison bison) (Ward et al., 1999; Dyer et al., 2001) and has been isolated from both healthy and diseased cattle (Nakaya et al., 1995; Blackall et al., 2007; Collins, 2011; Cortese et al., 2012), roe deer (Blackall et al., 2007), goats (Ward et al., 2002) and from adult chamois (Rupicapra rupicapra) with interstitial pneumonia (Richard et al., 1992).

Distribution

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Bibersteinia trehalosi is distributed worldwide.

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

JapanPresentNakaya et al., 1995
TurkeyPresentGüler et al., 1996; Kaya and Kirkan, 1999

Africa

EthiopiaPresentSisay and Zerihun, 2003
KenyaPresentMwangota et al., 1978
SudanPresentElsheikh and Hassan, 2012

North America

USAPresentPresent based on regional distribution.
-CaliforniaPresentTomassini et al., 2009
-ColoradoPresentWolfe et al., 2010
-IdahoPresentDunbar et al., 1990; Drew et al., 2014
-OregonPresentMiller et al., 2012
-WyomingPresentMiller et al., 2012

Europe

FrancePresentAbadie and Thiery, 2006; Villard et al., 2006
HungaryPresent
SpainPresentGonzalez et al., 2013
UKPresentWatson and Scholes, 2010; Collins, 2011

Oceania

AustraliaPresentPresent based on regional distribution.
-New South WalesPresentMackie et al., 1995
New ZealandPresentBlack, 1997

Pathology

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The systemic form of pasteurellosis caused by B. trehalosi is characterized by fever, listlessness, poor appetite, and sudden death in young sheep. The organism is thought to move from the tonsils to the lungs and pass into the blood. This results in septicaemia and localization of the infection in one or more tissues such as the joints, udder, meninges, or lungs.

Postmortem examinations sometimes reveal subcutaneous haemorrhages over the neck and thorax, with superficial haemorrhages on the pleura, diaphragm and epicardium. The lungs may be swollen with widespread haemorrhages, and bloodstained froth in the airways, but no evidence of consolidation. Necrotic erosions are sometimes seen in the pharynx around the tonsils, nasal mucosa, oesophagus and abomasum. The tonsils and retropharyngeal lymph nodes are enlarged. The abdominal viscera are often congested; in some cases, necrotic infarcts may also be present in the liver, spleen and kidney, visible as small grey foci (Sargison, 2009).

Diagnosis

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Clinical disease usually follows within a few days of exposure to predisposing factors; sudden death often occurs in the absence of premonitory clinical signs (Gilmour, 1978; Ellis, 1984). Occasionally, affected animals show a fever, reluctance to move, dyspnoea, blood-stained frothy discharge from the nose and mouth, and recumbency followed by death (Gilmour, 1978). The mortality rate seldom exceeds 5 percent.

Diagnosis of pneumonic and septicaemic forms of pasteurellosis is based on necropsy examination, gross and histopathologic findings, and isolation of organisms from a range of tissues, including lungs, liver and spleen (Ellis, 1984). Lesions include subcutaneous haemorrhage; epithelial necrosis of the tongue, pharynx, oesophagus, or occasionally the abomasum and intestine; enlargement of tonsils and retropharyngeal lymph nodes; and peracute, multifocal, embolic, necrotizing lesions in the lung and liver.

Disease Course

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Bibersteinia trehalosi is a common inhabitant of the upper respiratory tract and tonsils of healthy sheep. Local mucosal invasion and systemic spread are thought to follow a period of stress or management change (Dyson et al., 1981; Suàrez-Güémes et al., 1985). Stress is thought to result in corticosteroid-dependent bacterial proliferation in the tonsillar region, and injury to the alimentary tract, with consequent ulceration (Suàrez-Güémes et al., 1985). The injured pharyngeal, abomasal and duodenal mucosa serve as portals of entry for B. trehalosi derived from the tonsils. From these sites bacteria gain access to the blood as emboli, most of which impact in the capillary bed of the lungs (Dyson et al., 1981), whilst bacterial invasion of the lower alimentary tract results in primary embolization of the hepatic sinusoids (Suàrez-Güémes et al., 1985). Rapid multiplication of bacteria in these sites results in embolic dissemination to other organs and tissue. Death is attributed to endotoxaemia (Dyson et al., 1981; Suàrez-Güémes et al., 1985; Hodgson et al., 1993).

The virulence of B. trehalosi is mediated by the action of several factors, including endotoxin, adhesins, leukotoxin, and capsular polysaccharide, that afford the bacteria advantages over host immunity. The leukotoxin is particularly important in pathogenesis (Subramaniam et al., 2014). Typically, domestic sheep carry leukotoxin-positive Mannheimia haemolytica and/or B. trehalosi as commensal bacteria in their nasopharynx. In contrast, most bighorn sheep do not carry leukotoxin-positive M. haemolytica or B. trehalosi, or carry leukotoxin-negative strains in their nasopharynx (Subramaniam et al., 2014).

Dassanayake et al. (2010) describe the interaction between B. trehalosi and M. haemolytica. The authors point out that although B. trehalosi is commonly isolated from cases of pneumonia in bighorn sheep, M. haemolytica is the only pathogen that has consistently been shown to cause bronchopneumonia and death under experimental conditions. Other studies show that only leukotoxin-producing strains of B. trehalosi can cause pneumonia (Dassanayake et al., 2013). As a result, there is some question as to whether or not B. trehalosi is likely to be a major cause of pneumonia in bighorn sheep. Research by the authors shows that B. trehalosi replicates at almost twice the rate of M. haemolytica and is able to inhibit and overgrow M. haemolytica. This data would lead to speculation that, in many cases, M. haemolytica might be the initial cause of pneumonia but is then overgrown by B. trehalosi, which is the organism subsequently isolated.

Although B. trehalosi infections are considered rare in cattle, B. trehalosi is sometimes isolated from cattle with respiratory disease and reports seem to be increasing (Collins, 2011). Cortese et al. (2012) reported severe non-responsive bovine respiratory disease (BRD) outbreaks associated with multidrug-resistant B. trehalosi.

To evaluate the role of B. trehalosi in BRD, Hanthorn et al. (2014) used an intra-tracheal inoculation model in calves. They found that B. trehalosi-inoculated calves did not have increased lung involvement compared to control calves and concluded that B. trehalosi may not be a primary pathogen of respiratory disease in cattle. Culture of B. trehalosi from diagnostic submissions should not be immediately identified as a primary cause of respiratory disease, they say. They speculate that the main role of B. trehalosi in BRD may be as secondary and perhaps opportunistic bacteria.

B. trehalosi has been identified as the cause of necrotizing hepatitis/sudden death in an adult cow (Watson and Scholes, 2010). Spagnoli et al. (2011) describe a case of subcutaneous botryomycosis caused by B. trehalosi in a Texas Longhorn steer.

Epidemiology

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Although sheep of any age are susceptible to systemic pasteurellosis, animals five to 12 months old are at greatest risk (Dyson et al., 1981; Ellis, 1984). Prevalence increases in cold, wet weather conditions (Dyson et al., 1981). Stress associated with weaning, transportation, vaccination and shearing, as well as a change in diet, are thought to be predisposing factors (Suarez-Guemes, 1983; Suàrez-Güémes et al., 1985; Mackie et al., 1995). Concurrent diseases such as cobalt deficiency or tickborne fever (caused by Anaplasma phagocytophilum) may also predispose to outbreaks of the disease (Sargison, 2009; Daniel et al., 2015).

Disease Treatment

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Antimicrobials effective against gram-negative bacteria, such as ampicillin, amoxicillin-clavulinic acid, ceftiofur, oxytetracycline and florfenicol, can potentially be used to treat B. trehalosi infections, although strains vary in their susceptibility (Richard et al., 1992; Sanchis and Abadie, 1992; Weiser et al., 2009; Scott, 2011). However, sheep are rarely seen in the early stages of the disease and treatment is only successful if begun very early in the disease process due to rapid progression of lung damage and endotoxin release. Parenteral fluids and anti-inflammatory agents are important adjuncts to antibiotic therapy (Scott, 2011).

The presence of antimicrobial resistance genes in B. trehalosi was first reported by Kehrenberg et al. (2006) in a florfenicol-resistant isolate from a calf. They found that resistance to chloramphenicol and florfenicol were associated with a plasmid which also carried functionally active genes for resistance to sulphonamides.

Prevention and Control

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Immunization and Vaccines

In some countries, vaccines are available for small ruminants that offer some degree of immunity to Pasteurella haemolytica/Pasteurella trehalosi; most are combined with clostridial disease vaccines (Duncanson, 2012). The vaccine that is solely for pasteurellosis has to be given as two doses separated by 4-6 weeks. If there is an early threat to younger lambs, the first dose should be given at 2 weeks of age and the second at 6 weeks of age. Otherwise the timing should be adjusted so that the second dose is given a few days before the time of greatest threat. The Pasteurella component is much more expensive than the clostridial component of the combined vaccine, and so should only be given if there is a real need (Duncanson, 2012).

Bowersock et al. (2014) reported that a multivalent modified-live virus (MLV) vaccine containing M. haemolytica toxoid protected calves against challenge exposure with virulent B. trehalosi by reducing the mortality rate, lung lesion scores, and clinical scores for respiratory disease.

Husbandry methods and good practice

While vaccines offer the best means of disease control, stress likely plays a part in predisposing to disease. Flock management should be designed to minimize the stress involved in changes of environment and nutrition (Dyson et al., 1981; Suàrez-Güémes et al., 1985).

References

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Abadie G; Thiery R, 2006. Pasteurellosis in small ruminants: update of Mannheimia haemolytica and Pasteurella trehalosi serotyping. (Pasteurelloses des petits ruminants: actualité en matière de sérotypage de Mannheimia haemolytica et de Pasteurella trehalosi.) Revue de Médecine Vétérinaire, 157(11):530-534.

Al-Sultan II; Aitken ID, 1985. The tonsillar carriage of Pasteurella haemolytica in lambs. Journal of Comparative Pathology, 95(2):193-201.

Angen O; 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.

Black H, 1997. Pasteurella isolates from sheep pneumonia cases in New Zealand. Surveillance (Wellington), 24(3):5-8.

Blackall PJ; Bojesen AM; 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

Bowersock TL; Sobecki BE; Terrill SJ; Martinon NC; Meinert TR; Leyh RD, 2014. Efficacy of a multivalent modified-live virus vaccine containing a Mannheimia haemolytica toxoid in calves challenge exposed with Bibersteinia trehalosi. American Journal of Veterinary Research, 75(8):770-776. http://avmajournals.avma.org/doi/abs/10.2460/ajvr.75.8.770

Collins RL, 2011. Bibersteinia trehalosi in cattle - another component of the bovine respiratory disease complex? Cattle Practice [BCVA Congress 2010, Torquay, UK, 14-16 October 2010.], 19(1):9-12. http://www.bcva.org.uk

Confer AW; Panciera RJ; Clinkenbeard KD; Mosier DA, 1990. Molecular aspects of virulence of Pasteurella haemolytica. Canadian Journal of Veterinary Research, 54(Supplement):S48-S52.

Cortese VS; Braun DA; Crouch D; Townsend C; Zukowski B, 2012. Case report - peracute to acute fatal pneumonia in cattle caused by Bibersteinia trehalosi. Bovine Practitioner [45th Annual Conference of the American Association of Bovine Practitioners, Montreal, Canada, 20-22 September 2012.], 46(2):138-142. http://www.aabp.org

Daniel R; Pugh K; Torrens N; Carson A; Wessels M, 2015. Intercurrent tickborne fever infection and Bibersteinia trehalosi septicaemia in a five-week-old lamb. Veterinary Record, 177(1):24.

Dassanayake RP; Call DR; Sawant AA; Casavant NC; Weiser GC; Knowles DP; Srikumaran S, 2010. Bibersteinia trehalosi inhibits the growth of Mannheimia haemolytica by a proximity-dependent mechanism. Applied and Environmental Microbiology, 76(4):1008-1013. http://aem.asm.org

Dassanayake RP; Shanthalingam S; Subramaniam R; Herndon CN; Bavananthasivam J; Haldorson GJ; Foreyt WJ; Evermann JF; Herrmann-Hoesing LM; Knowles DP; Srikumaran S, 2013. Role of Bibersteinia trehalosi, respiratory syncytial virus, and parainfluenza-3 virus in bighorn sheep pneumonia. Veterinary Microbiology, 162(1):166-172. http://www.sciencedirect.com/science/journal/03781135

Davies RL; Arkinsaw S; Selander RK, 1997. Genetic relationships among Pasteurella trehalosi isolates based on multilocus enzyme electrophoresis. Microbiology (Reading), 143(8):2841-2849.

Donachie W, 2007. Pasteurellosis. In: Diseases of Sheep, 4th edition [ed. by Aitken, I.]. Ames, Iowa, USA: Blackwell Publishing, 224-231.

Drew ML; Rudolph KM; Ward ACS; Weiser GC, 2014. Health status and microbial (Pasteurellaceae) flora of free-ranging bighorn sheep following contact with domestic ruminants. Wildlife Society Bulletin, 38(2):332-340. http://onlinelibrary.wiley.com/doi/10.1002/wsb.393/full

Dunbar MR; Ward ACS; Power G, 1990. Isolation of Pasteurella haemolytica from tonsillar biopsies of rocky mountain bighorn sheep. Journal of Wildlife Diseases, 26(2):210-213.

Duncanson GR, 2012. Vaccines. In: Veterinary treatment of sheep and goats [ed. by Duncanson, G. R.]. Wallingford, UK: CAB International, 94-102. http://www.cabi.org/cabebooks/ebook/20123130344

Dyer NW; Ward ACS; Weiser GC; White DG, 2001. Seasonal incidence and antibiotic susceptibility patterns of Pasteurellaceae isolated from American bison (Bison bison). Canadian Journal of Veterinary Research, 65(1):7-14.

Dyson DA; Gilmour NJL; Angus KW, 1981. Ovine systemic pasteurellosis caused by Pasteurella haemolytica biotype T. Journal of Medical Microbiology, 14(1):89-95.

Ellis JA, 1984. Pasteurella haemolytica infections in sheep. Compendium on Continuing Education for the Practicing Veterinarian, 6(6):S360-S367.

Elsheikh HM; Hassan SO, 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

Fodor L; Varga J; Hajtós I; Molnár T, 1999. Serotypes of Pasteurella haemolytica and Pasteurella trehalosi isolated from farm animals in Hungary. Journal of Veterinary Medicine. Series B, 46(4):241-247.

Gilmour NJL, 1978. Pasteurellosis in sheep. Veterinary Record, 102(5):100-102.

Gonzalez JM; Lacasta D; Ferrer LM; Figueras L; Abadie G; Heras Mde las, 2013. Mannheimia haemolytica and Bibersteinia trehalosi serotypes isolated from lambs with ovine respiratory complex in Spain. Deltion tes Ellenikes Kteniatrikes Etaireias = Journal of the Hellenic Veterinary Medical Society, 64(3):177-182.

Guillou Sle, 2004. Caprine pasteurellosis: a major pulmonary disease in young goats. (Pasteurellose caprine: une maladie pulmonaire dominante chez les jeunes.) Chèvre, No.262:31-32.

Güler L; Baysal T; Gündüz K; Erganis O; Kaya O; Orhan G, 1996. Biotyping and serotyping of Pasteurella haemolytica strains isolated from sheep and goats. (Koyun ve keçilerden izole edilen Pasteurella haemolytica suslarinin biyotip ve serotiplendirilmesi.) Veterinarium, 7(1/2):5-12.

Hanthorn CJ; Dewell RD; Cooper VL; Frana TS; Plummer PJ; Wang C; Dewell GA, 2014. Randomized clinical trial to evaluate the pathogenicity of Bibersteinia trehalosi in respiratory disease among calves. BMC Veterinary Research, 10(89):(18 April 2014). http://www.biomedcentral.com/content/pdf/1746-6148-10-89.pdf

Hodgson JC; Moon GM; Quirie M; Donachie W, 1994. Biochemical signs of endotoxaemia in lambs challenged with T10 strain of Pasteurella haemolytica and the effect of vaccination on the host response. In: Science serving sheep: Volume 17. Proceedings Third International Sheep Veterinary Conference 1993 [ed. by Goodier, J.\Spence, J.]. Edinburgh, UK: Sheep Veterinary Society, 201-204.

Kaya O; Kirkan S, 1999. Biotyping and antimicrobial susceptibility of Pasteurella haemolytica strains isolated from the nasal cavity of normal and pneumonic sheep in Aydin Region. (Aydin bölgesindeki saglikli ve pnömoni süpheli koyunlardan Pasteurella haemolytica 'nin izolasyonu, biyotip tayini ve antibiyotiklere duyarliliklari.) Bornova Veteriner Kontrol ve Arastirma Enstitüsü Dergisi, 24(38):21-25.

Kehrenberg C; Meunierle D; Targant H; Cloeckaert A; Schwarz S; Madec JY, 2006. Plasmid-mediated florfenicol resistance in Pasteurella trehalosi. Journal of Antimicrobial Chemotherapy, 58(1):13-17. http://jac.oxfordjournals.org/cgi/content/abstract/58/1/13

Mackie JT; Barton M; Hindmarch M; Holsworth I, 1995. Pasteurella haemolytica septicaemia in sheep. Australian Veterinary Journal, 72(12):474; 13 ref.

Miller DS; Weiser GC; Ward ACS; Drew ML; Chapman PL, 2011. Domestic sheep (Ovis aries) pasteurellaceae isolates from diagnostic submissions to the Caine Veterinary Teaching Center (1990-2004). Veterinary Microbiology, 150(3/4):284-288. http://www.sciencedirect.com/science/journal/03781135

Miller DS; Weiser GC; Ward ACS; Drew ML; Chapman PL, 2012. Pasteurellaceae isolated from bighorn sheep (Ovis canadensis) from Idaho, Oregon, and Wyoming. American Journal of Veterinary Research, 73(7):1024-1028. http://www.avma.org/journals/default.asp

Mwangota AU; Muhammed SI; Thomson RG, 1978. Serological types of Pasteurella haemolytica in Kenya. Cornell Veterinarian, 68(1):84-93.

Nakaya I; Nakazawa M; Hashimoto Y; Ikeuchi T; Noma S; Torikai Y; Ezaki T, 1995. Isolation and characterization of Pasteurella trehalosi from cattle. Journal of the Japan Veterinary Medical Association, 48(10):750-754.

Richard Y; Borges E; Gauthier D; Favier C; Sanchis R; Oudar J, 1992. Isolation of 33 strains of beta-haemolytic Pasteurella of the haemolytica-trehalosi group from chamois (Rupicapra rupicapra). (Isolement de 33 souches de Pasteurella beta hémolytiques du groupe: haemolytica-trehalosi chez le chamois (Rupicapra rupicapra).) Gibier Faune Sauvage, 9(Mars):71-85.

Rudolph KM; Hunter DL; Rimler RB; Cassirer EF; Foreyt WJ; DeLong WJ; Weiser GC; Ward ACS, 2007. Microorganisms associated with a pneumonic epizootic in rocky mountain bighorn sheep (Ovis canadensis canadensis). Journal of Zoo and Wildlife Medicine, 38(4):548-558.

Sanchis R; Abadie G, 1992. Antibiotic sensitivity of Pasteurella haemolytica and P. trehalosi strains isolated from sheep and goats in France. (A study of 262 strains). (Sensibilité aux antibiotiques des Pasteurella haemolytica et trehalosi d'origine ovine et caprine isolées en France. (Étude de 262 souches).) Recueil de Médecine Vétérinaire, 168(10):807-813.

Sanchis R; Guerrault P; Abadie G; Pellet MP, 1991. Frequency of isolation of serotypes of Pasteurella haemolytica from sheep and goats. Study of 230 strains. (Fréquence d'isolement des sérotypes de Pasteurella haemolytica chez les ovins et les caprins. Étude de 230 souches.) Revue de Médecine Vétérinaire, 142(3):201-205.

Sargison N, 2009. Sheep flock health: a planned approach [ed. by Sargison, N.]. Chichester, UK: Wiley-Blackwell, 465 pp. http://onlinelibrary.wiley.com/book/10.1002/9781444302592

Scott P, 2011. Diagnosis and treatment of respiratory disease in adult sheep. UK Vet: Livestock, 16(4):36-39. http://www.ukvet.co.uk

Sisay T; Zerihun A, 2003. Diversity of Mannheimia haemolytica and Pasteurella trehalosi serotypes from apparently healthy sheep and abattoir specimens in the highlands of Wollo, North East Ethiopia. Veterinary Research Communications, 27(1):3-14.

Sneath PH; Stevens M, 1990. Actinobacillus rossii sp. nov., Actinobacillus seminis sp. nov., nom. rev., Pasteurella bettii sp. nov., Pasteurella lymphangitidis sp. nov., Pasteurella mairi sp. nov., and Pasteurella trehalosi sp. nov. International Journal of Systematic Bacteriology, 40(2):148-153.

Spagnoli S; Reilly TJ; Calcutt MJ; Fales WH; Kim DY, 2012. Subcutaneous botryomycosis due to Bibersteinia trehalosi in a Texas Longhorn steer. Veterinary Pathology, 49(5):775-778. http://vet.sagepub.com/content/49/5/775.abstract

Suarez-Guemes F, 1983. Septicemic pasteurellosis in feedlot lambs. Dissertation Abstracts International, B, 44(4):1016.

Suàrez-Güémes F; Collins MT; Whiteman CE, 1985. Experimental reproduction of septicemic pasteurellosis in feedlot lambs: bacteriologic and pathologic examinations. American Journal of Veterinary Research, 46(1):193-201.

Subramaniam R; Shanthalingam S; Bavananthasivam J; Kugadas A; Raghavan B; Batra SA; Herndon CN; Rodriguez J; Tibary A; Nelson D; Potter KA; Foreyt WJ; Srikumaran S, 2014. Bighorn sheep × domestic sheep hybrids survive Mannheimia haemolytica challenge in the absence of vaccination. Veterinary Microbiology, 170(3/4):278-283. http://www.sciencedirect.com/science/journal/03781135

Tomassini L; Gonzales B; Weiser GC; Sischo W, 2009. An ecologic study comparing distribution of Pasteurella trehalosi and Mannheimia haemolytica between Sierra Nevada bighorn sheep, White Mountain bighorn sheep, and domestic sheep. Journal of Wildlife Diseases, 45(4):930-940. http://www.wildlifedisease.org

Villard L; Gauthier D; Lacheretz A; Abadie G; Game Y; Maurin F; Richard Y; Borges E; Kodjo A, 2006. Serological and molecular comparison of Mannheimia haemolytica and Pasteurella trehalosi strains isolated from wild and domestic ruminants in the French Alps. Veterinary Journal, 171(3):545-550.

Ward ACS; Dyer NW; Fenwick BW, 1999. Pasteurellaceae isolated from tonsillar samples of commercially-reared American bison (Bison bison). Canadian Journal of Veterinary Research, 63(3):161-165; 36 ref.

Ward ACS; Weiser GC; DeLong WJ; Frank GH, 2002. Characterization of Pasteurella spp. isolated from healthy domestic pack goats and evaluation of the effects of a commercial Pasteurella vaccine. American Journal of Veterinary Research, 63(1):119-123.

Watson PJ; Scholes SFE, 2010. Bibersteinia trehalosi necrotising hepatitis associated with sudden death in an adult cow. Veterinary Record, 167(3):100-102. http://veterinaryrecord.bvapublications.com/archive/

Weiser GC; Miller DS; Drew ML; Rhyan JC; Ward ACS, 2009. Variation in Pasteurella (Bibersteinia) and Mannheimia spp. following transport and antibiotic treatment in free-ranging and captive rocky mountain bighorn sheep (Ovis canadensis canadensis). Journal of Zoo and Wildlife Medicine, 40(1):117-125.

Wolfe LL; Diamond B; Spraker TR; Sirochman MA; Walsh DP; Machin CM; Bade DJ; Miller MW, 2010. A bighorn sheep die-off in southern Colorado involving a Pasteurellaceae strain that may have originated from syntopic cattle. Journal of Wildlife Diseases, 46(4):1262-1268. http://www.wildlifedisease.org

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