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tularaemia

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tularaemia

Summary

  • Last modified
  • 14 July 2018
  • Datasheet Type(s)
  • Animal Disease
  • Preferred Scientific Name
  • tularaemia
  • Overview
  • Tularaemia is a zoonotic disease caused by Francisella tularensis, a bacterium with a broad host range, including mammals, birds and invertebrates (

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Identity

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Preferred Scientific Name

  • tularaemia

Other Scientific Names

  • tularemia

International Common Names

  • English: tularemia in sheep, horses, and swine

Overview

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Tularaemia is a zoonotic disease caused by Francisella tularensis, a bacterium with a broad host range, including mammals, birds and invertebrates (Ellis et al., 2002; Keim et al., 2007). F. tularensis is thought to be maintained in the environment principally by various terrestrial and aquatic mammals such as rabbits, hares, ground squirrels, voles, muskrats, water rats and other rodents (Mörner, 1992). Tularaemia is rare in domestic animals, but clinical cases occur in cats (Rhyan et al., 1990; Gliatto et al., 1994), and occasional outbreaks have been reported among cattle (Geiger, 1931; Philip and Williams, 1985), sheep (Geiger, 1931; Jellison et al., 1965; O'Toole et al., 2008), captive prairie dogs (Lindley et al., 2002) and ranched mink (Henson, et al., 1978). Tularaemia is on the OIE list of notifiable diseases. Due to its high virulence and zoonotic potential, F. tularensis is listed as a category A select bioterrorism agent (Foley and Nieto, 2010).

In humans, tularaemia can be a serious and potentially life-threatening disease. F. tularensis can be transmitted to humans through multiple routes, including contact with animals or contaminated environments, or through arthropod vectors (Foley and Nieto, 2010; Thomas, and Schaffner, 2010). Clinical manifestations depend on the infection route, and the disease severity depends on the infecting subspecies and strain (Ellis et al., 2002; Thomas and Schaffner, 2010). Ulceroglandular tularaemia, the most common form of disease, results from exposure through the skin (either pre-existing wound or arthropod bite). This form usually results in an ulcer at the site of infection followed by lymphadenopathy. Pneumonic tularaemia, the most serious form of disease, results from inhalation of aerosolized bacteria. Other forms of the disease include oculoglandular (exposure via the eye), oropharyngeal (ingestion), and typhoidal tularaemia (systemic infection without a primary ulcer).

The history of tularaemia is reviewed by Sjöstedt, 2007. F. tularensis was first isolated from a ground squirrel in 1911 in Tulare County, California, USA. It was first named Bacterium tularense, later reclassified as Pasteurella tularense/Pasteurella tularensis, and in 1966 was named Francisella tularensis. Descriptions of a disease now considered to be tularaemia predate this first isolation, going as far back as 1818 in Japan. The first laboratory-confirmed human case was reported in 1914. Colloquial names such as rabbit fever, hare fever, deerfly fever and lemming fever have been used to describe the disease (Mörner, 1992).

F. tularensis is ubiquitous in the Northern Hemisphere and there are four subspecies: F. tularensis subsp. tularensis (type A), F. tularensis subsp. holarctica (type B), F. tularensis subsp. mediasiatica and F. tularensis subsp. novicida [although it has been suggested that the latter is a separate species, F. novicida]. Types A and B are considered most important for causing disease in humans and animals. Type A, the most virulent of the subspecies, is present almost exclusively in North America and type B is distributed all over the Northern Hemisphere, but predominately in Asia and Europe. F. tularensis subsp. mediasiatica has only been isolated in Kazakhstan and Turkmenistan in Central Asia (Keim et al., 2007). F. tularensis subsp. novicida has been reported from North America and Australia (Whipp et al., 2003; Siddaramappa et al., 2011; Brett et al., 2014).

Hosts/Species Affected

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Francisella tularensis has a broad host range, which includes mammals, invertebrates and birds, but it is thought to be maintained in the environment primarily by terrestrial and aquatic mammals (Mörner, 1992; Ellis et al., 2002; Sjöstedt, 2007). In regions where tularaemia is endemic, antibodies to F. tularensis are frequently detected in the sera of trapped wild animals and outbreaks of disease in humans often parallel outbreaks of tularaemia in wild animals (reviewed by Ellis et al., 2002; Sjöstedt, 2007).

Many small mammals, particularly hares and rodents, have been found infected with tularaemia in European and Asian countries. The brown hare (Lepus europaeus) is considered the major source of human tularaemia in central Europe (Keim et al., 2007; Müller et al., 2013). Infection is acquired by direct contact, often from skinning the animals (Otto et al., 2015). The mountain hare (Lepus timidus) is distributed in colder areas: alpine continental Europe, Fennoscandia (Sweden, Finland, Norway), and Russia. Hunter-associated tularaemia occurs with mountain hares but seems less common, possibly because these animals are very susceptible to tularaemia and rapidly die before they can be harvested (Mörner, 1992).

Cricetine rodents (voles) are believed to be of major importance for maintaining tularaemia in Eurasia. Arvicola terrestris (the water vole) and Microtus arvalis (the common vole) are the species most frequently involved in tularaemia epizootics and have been studied extensively, but many more species also are found infected (Mörner, 1992; Keim et al., 2007).

In North America, lagomorphs of the genera Sylvilagus (cottontail rabbits) are widely recognized as important hosts of tularaemia (Mörner, 1992; Sinclair et al., 2008). Because of this, tularaemia is commonly known as “rabbit fever” in many regions of the United States. After bites from arthropods, skinning of rabbits is considered one of the most common sources of human infections, particularly in the south-central United States (Taylor et al., 1991) where most human cases are concentrated.

In North America, F. tularensis subsp. holarctica has been linked to voles (Microtus spp.) and semiaquatic mammals, such as American beavers (Castor canadensis) and muskrats (Ondatra zibethicus) (Hopla, 1974; Keim et al., 2007).

In Japan, human infection with F. tularensis subsp. holarctica is associated with hunting of the Japanese hare (Lepus brachyurus) (Ohara et al., 1996).

Among domesticated animals, sheep and cats are particularly susceptible to clinical disease. Tularaemia has also been seen in dogs (Meinkoth et al., 2004; Nordstoga et al., 2014), pigs (Pashov, 1956), horses (Claus et al., 1959), nonhuman primates (Beckwith, 2006; Gyuranecz et al., 2009), farmed mink (Henson et al., 1978), captive prairie dogs (Lindley et al., 2002; Petersen, et al., 2004) and cattle (Geiger, 1931; Philip and Williams, 1985). Natural infections have also been reported in birds, fish, amphibians and invertebrates (Mörner, 1992).

Humans are highly susceptible to infection, resulting in a disease that ranges from mild to severe (Ellis et al., 2002).

Distribution

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F. tularensis is ubiquitous in the Northern Hemisphere (Sjöstedt, 2007). F. tularensis subsp. tularensis (type A) is present almost exclusively in North America. F. tularensis subsp. holarctica (type B) is distributed all over the Northern Hemisphere, but predominately in Asia and Europe. F. tularensis subsp. mediasiatica has only been isolated in Kazakhstan and Turkmenistan in Central Asia (Sandström et al., 1992; Keim et al., 2007). F. tularensis subsp. novicida has been reported from North America and Australia (Whipp et al., 2003; Siddaramappa et al., 2011; Brett et al., 2014).

Tularaemia has recently emerged in some areas (reviewed by Petersen and Schriefer, 2005). It was recognized for the first time in Spain in 1997-1998, when two outbreaks, one associated with hares (García del Blanco et al., 2004) and the other linked to crayfish (Anda et al., 2001), affected more than 500 people. In 2000, a human epidemic in Kosovo was associated with a population explosion and epizootic among rodents, which occurred after large numbers of people had been displaced from their homes by the conflict (Reintjes et al., 2002; Zajmi et al., 2013). In 2002, an outbreak was seen among captive prairie dogs in the USA (Lindley et al., 2002), and the disease entered the Czech Republic in a shipment of these animals (Petersen, et al., 2004). Tularaemia was detected for the first time in the Southern Hemisphere the same year, when a case caused by F. tularensis subsp. novicida was identified in Australia (Whipp et al., 2003). F. tularensis seems to be a re-emerging pathogen in Germany (Kaysser et al., 2008; Müller et al., 2013).

For current information on disease distribution, see OIE's WAHID Interface.

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

AfghanistanNo information availableOIE, 2009
ArmeniaDisease not reportedOIE, 2009
AzerbaijanDisease not reportedOIE, 2009
BahrainDisease never reportedOIE, 2009
BangladeshDisease never reportedOIE, 2009
BhutanDisease never reportedOIE, 2009
Brunei DarussalamDisease not reportedOIE Handistatus, 2005
CambodiaNo information availableOIE, 2009
ChinaPresentOIE, 2009; Wang et al., 2014
-Hong KongNo information availableOIE, 2009
Georgia (Republic of)Disease never reportedOIE Handistatus, 2005
IndiaNo information availableOIE, 2009
IndonesiaDisease not reportedOIE, 2009
IranPresentOIE, 2009; Esmaeili et al., 2014
IraqNo information availableOIE, 2009
IsraelDisease never reportedOIE, 2009
JapanDisease not reportedOhara et al., 1996; Ohara et al., 1998; OIE, 2009
JordanNo information availableOIE, 2009
KazakhstanDisease not reportedOIE, 2009
Korea, DPRDisease not reportedOIE Handistatus, 2005
Korea, Republic ofDisease never reportedOIE, 2009
KuwaitDisease not reportedOIE, 2009
KyrgyzstanDisease not reportedOIE, 2009
LaosNo information availableOIE, 2009
LebanonDisease not reportedOIE, 2009
MalaysiaDisease never reportedOIE, 2009
-Peninsular MalaysiaDisease not reportedOIE Handistatus, 2005
-SabahDisease never reportedOIE Handistatus, 2005
-SarawakDisease never reportedOIE Handistatus, 2005
MongoliaNo information availableOIE, 2009
MyanmarNo information availableOIE, 2009
NepalDisease not reportedOIE, 2009
OmanDisease never reportedOIE, 2009
PakistanDisease not reportedOIE, 2009
PhilippinesNo information availableOIE, 2009
QatarNo information availableOIE, 2009
Saudi ArabiaNo information availableOIE, 2009
SingaporeDisease never reportedOIE, 2009
Sri LankaDisease never reportedOIE, 2009
SyriaDisease never reportedOIE, 2009
TaiwanDisease never reportedOIE Handistatus, 2005
TajikistanDisease not reportedOIE, 2009
ThailandNo information availableOIE, 2009
TurkeyPresentOIE, 2009; Büyük et al., 2012; Erdem et al., 2014
TurkmenistanDisease not reportedOIE Handistatus, 2005
United Arab EmiratesDisease not reportedOIE, 2009
UzbekistanDisease not reportedOIE Handistatus, 2005
VietnamNo information availableOIE, 2009
YemenNo information availableOIE, 2009

Africa

AlgeriaDisease not reportedOIE, 2009
AngolaNo information availableOIE, 2009
BeninNo information availableOIE, 2009
BotswanaDisease never reportedOIE, 2009
Burkina FasoNo information availableOIE, 2009
BurundiNo information availableOIE Handistatus, 2005
CameroonNo information availableOIE Handistatus, 2005
Cape VerdeDisease never reportedOIE Handistatus, 2005
Central African RepublicDisease not reportedOIE Handistatus, 2005
ChadNo information availableOIE, 2009
CongoNo information availableOIE, 2009
Congo Democratic RepublicDisease not reportedOIE Handistatus, 2005
Côte d'IvoireDisease not reportedOIE Handistatus, 2005
DjiboutiNo information availableOIE, 2009
EgyptNo information availableOIE, 2009
EritreaNo information availableOIE, 2009
EthiopiaNo information availableOIE, 2009
GabonNo information availableOIE, 2009
GambiaNo information availableOIE, 2009
GhanaNo information availableOIE, 2009
GuineaNo information availableOIE, 2009
Guinea-BissauNo information availableOIE, 2009
KenyaDisease never reportedOIE, 2009
LesothoDisease never reportedOIE, 2009
LibyaDisease never reportedOIE Handistatus, 2005
MadagascarDisease never reportedOIE, 2009
MalawiNo information availableOIE, 2009
MaliNo information availableOIE, 2009
MauritiusDisease not reportedOIE, 2009
MoroccoNo information availableOIE, 2009
MozambiqueNo information availableOIE, 2009
NamibiaNo information availableOIE, 2009
NigeriaNo information availableOIE, 2009
RéunionDisease never reportedOIE Handistatus, 2005
RwandaDisease never reportedOIE, 2009
Sao Tome and PrincipeDisease not reportedOIE Handistatus, 2005
SenegalNo information availableOIE, 2009
SeychellesDisease not reportedOIE Handistatus, 2005
SomaliaNo information availableOIE Handistatus, 2005
South AfricaDisease never reportedOIE, 2009
SudanDisease never reportedOIE, 2009
SwazilandNo information availableOIE, 2009
TanzaniaDisease never reportedOIE, 2009
TogoNo information availableOIE, 2009
TunisiaDisease not reportedOIE, 2009
UgandaNo information availableOIE, 2009
ZambiaDisease not reportedOIE, 2009
ZimbabweDisease never reportedOIE, 2009

North America

BermudaDisease not reportedOIE Handistatus, 2005
CanadaAbsent, reported but not confirmedOIE, 2009; Wobeser et al., 2009; Blackburn et al., 2013
GreenlandDisease never reportedOIE, 2009
MexicoDisease not reportedOIE, 2009
USAAbsent, reported but not confirmedTaylor et al., 1991; OIE, 2009
-AlaskaPresentHansen et al., 2011
-ArkansasPresentMagee et al., 1989; Taylor et al., 1991
-CaliforniaPresentGEIGER, 1931
-ConnecticutPresentMagnarelli et al., 2007
-IdahoPresentGEIGER, 1931
-IllinoisPresentShoemaker et al., 1997
-KansasPresentTaylor et al., 1991
-LouisianaPresentBrett et al., 2014
-MassachusettsPresentGliatto et al., 1994
-MinnesotaPresentScheftel et al., 2010
-MissouriPresentTaylor et al., 1991
-MontanaPresentGEIGER, 1931; Jellison et al., 1965
-NebraskaPresentLarson et al., 2014
-New YorkPresentMagnarelli et al., 2007
-OklahomaPresentTaylor et al., 1991
-PennsylvaniaPresentSinclair et al., 2008
-South DakotaPresentO'Toole et al., 2008
-TennesseePresentEvans et al., 1985
-TexasPresentLindley et al., 2002; Avashia et al., 2004
-UtahPresentCalanan et al., 2010
-WyomingPresentO'Toole et al., 2008

Central America and Caribbean

BarbadosDisease never reportedOIE Handistatus, 2005
BelizeNo information availableOIE, 2009
British Virgin IslandsDisease never reportedOIE Handistatus, 2005
Cayman IslandsDisease never reportedOIE Handistatus, 2005
Costa RicaDisease never reportedOIE, 2009
CubaDisease never reportedOIE, 2009
CuraçaoDisease not reportedOIE Handistatus, 2005
DominicaDisease not reportedOIE Handistatus, 2005
Dominican RepublicDisease never reportedOIE, 2009
El SalvadorDisease never reportedOIE, 2009
GuadeloupeNo information availableOIE, 2009
GuatemalaDisease never reportedOIE, 2009
HaitiDisease never reportedOIE, 2009
HondurasDisease never reportedOIE, 2009
JamaicaNo information availableOIE, 2009
MartiniqueNo information availableOIE, 2009
NicaraguaDisease never reportedOIE, 2009
PanamaDisease never reportedOIE, 2009
Saint Kitts and NevisDisease never reportedOIE Handistatus, 2005
Saint Vincent and the GrenadinesDisease never reportedOIE Handistatus, 2005
Trinidad and TobagoDisease never reportedOIE Handistatus, 2005

South America

ArgentinaDisease not reportedOIE, 2009
BoliviaDisease never reportedOIE, 2009
BrazilDisease never reportedOIE, 2009
ChileDisease never reportedOIE, 2009
ColombiaDisease never reportedOIE, 2009
EcuadorDisease never reportedOIE, 2009
Falkland IslandsDisease never reportedOIE Handistatus, 2005
French GuianaNo information availableOIE, 2009
GuyanaDisease never reportedOIE Handistatus, 2005
ParaguayDisease never reportedOIE Handistatus, 2005
PeruDisease never reportedOIE, 2009
UruguayDisease never reportedOIE, 2009
VenezuelaDisease never reportedOIE, 2009

Europe

AlbaniaDisease never reportedOIE, 2009
AndorraDisease not reportedOIE Handistatus, 2005
AustriaNo information availableOIE, 2009
BelarusNo information availableOIE, 2009
BelgiumDisease not reportedOIE, 2009
Bosnia-HercegovinaDisease not reportedOIE Handistatus, 2005
BulgariaPresentOIE, 2009; Padeshki et al., 2010
CroatiaPresentOIE, 2009; Gürcan, 2014
CyprusDisease never reportedOIE, 2009
Czech RepublicPresentHubálek and Halouzka, 1997; OIE, 2009; Gürcan, 2014
DenmarkDisease never reportedOIE, 2009
EstoniaNo information availableOIE, 2009
FinlandPresentSyrjälä et al., 1985; OIE, 2009; Rossow et al., 2014
FrancePresentOIE, 2009; Decors et al., 2011; Maurin et al., 2011
GermanyPresentKaysser et al., 2008; OIE, 2009; Müller et al., 2013
GreeceDisease not reportedOIE, 2009
HungaryPresentOIE, 2009; Gyuranecz et al., 2012
IcelandDisease never reportedOIE, 2009
IrelandDisease not reportedOIE, 2009
Isle of Man (UK)Disease never reportedOIE Handistatus, 2005
ItalyNo information availableErcolini et al., 1991; OIE, 2009
JerseyDisease never reportedOIE Handistatus, 2005
LatviaDisease never reportedOIE, 2009
LiechtensteinDisease not reportedOIE, 2009
LithuaniaDisease never reportedOIE, 2009
LuxembourgDisease not reportedOIE, 2009
MacedoniaAbsent, reported but not confirmedOIE, 2009
MaltaDisease never reportedOIE, 2009
MoldovaLast reported1996OIE Handistatus, 2005
MontenegroDisease not reportedOIE, 2009
NetherlandsDisease not reportedOIE, 2009
NorwayPresentBerdal et al., 1996; OIE, 2009; Nordstoga et al., 2014
PolandPresentOIE, 2009; Moniuszko et al., 2011
PortugalDisease not reportedOIE, 2009
RomaniaDisease never reportedOIE, 2009
Russian FederationAbsent, reported but not confirmedSandström et al., 1992; Efimov et al., 2003; OIE, 2009
SerbiaDisease not reportedReintjes et al., 2002; OIE, 2009; Zajmi et al., 2013
SlovakiaPresentGurycová et al., 2001; OIE, 2009; Gürcan, 2014
SloveniaDisease not reportedOIE, 2009
SpainRestricted distributionAnda et al., 2001; García et al., 2004; OIE, 2009
SwedenPresentBorg et al., 1969; Mörner et al., 1988; OIE, 2009; Rydén et al., 2012
SwitzerlandPresentFriedl et al., 2005; OIE, 2009
UKDisease not reportedOIE, 2009
-Northern IrelandDisease never reportedOIE Handistatus, 2005
UkraineDisease never reportedPASHOV, 1956; OIE, 2009
Yugoslavia (former)No information availableOIE Handistatus, 2005
Yugoslavia (Serbia and Montenegro)No information availableOIE Handistatus, 2005

Oceania

AustraliaPresentOIE, 2009; Siddaramappa et al., 2011
-Australian Northern TerritoryPresentWhipp et al., 2003
-TasmaniaPresentJackson et al., 2012
French PolynesiaDisease never reportedOIE, 2009
New CaledoniaDisease never reportedOIE, 2009
New ZealandDisease never reportedOIE, 2009
SamoaDisease never reportedOIE Handistatus, 2005
VanuatuDisease never reportedOIE Handistatus, 2005
Wallis and Futuna IslandsNo information availableOIE Handistatus, 2005

Pathology

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[From the OIE Terrestrial Manual, 2014, chapter 2.1.18 Tularemia (pdf)]

At necropsy, animals that have died from acute tularaemia are usually in good body condition. There are signs of septicaemia characterised by whitish foci of necrosis randomly distributed in the liver, bone marrow and spleen. In addition, the spleen is usually enlarged. Necrotic foci vary in size, and in some cases may be barely visible to the naked eye. The lungs are usually congested and oedematous, and there may be areas of consolidation and fibrinous pneumonia or pleuritis. Fibrin may be present in the abdominal cavity. Foci of caseous necrosis are often present in one or more lymph node(s). The lymph nodes that are most often affected are those in the abdominal and pleural cavities and lymph nodes draining the extremities. In less sensitive species, the histological picture can resemble that of tuberculosis with chronic granulomas in liver, spleen, lungs and kidneys.

Diagnosis

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[Also refer to the OIE Terrestrial Manual, 2014: chapter 2.1.18 Tularemia (pdf)]

As F. tularensis is zoonotic, samples must be collected, handled and shipped with care. Precautions should be taken including the wearing of gloves, masks and eyeshields.

The bacterium can be demonstrated in impression smears or in fixed specimens of organs, such as liver, spleen, bone marrow, kidney and lung, as well as in blood smears. Immunological methods, such as the fluorescent antibody test (FAT) are the most reliable way to identify the bacterium. With Gram staining, the bacteria appear as very small punctiform Gram-negative rods, often difficult to distinguish as bacteria. They can also be stained with May-Grunwald-Giemsa or phenol thionin. The organism is highly fastidious. For growth it is necessary to use Francis medium, McCoy and Chapin medium, or Modified Thayer-Martin agar.

Polymerase chain reaction (PCR) protocols have been developed for the rapid identification of F. tularensis in both clinical and environmental specimens (Fulop et al., 1996; Collazos Martínez et al., 2009; Birdsell et al., 2014).

Serology tests such as tube agglutination, microagglutination and enzyme-linked immunosorbent assays (ELISA) are useful for diagnosing human infection, but are of limited value in animals. Species sensitive to tularaemia typically die before specific antibodies develop; however, significant titres may be found in more resistant animals such as sheep, cattle, pigs and dogs (Long and Clifford, 1978; Ercolini et al., 1991; Splettstoesser et al., 2010; Büyük et al., 2012).

List of Symptoms/Signs

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SignLife StagesType
Cardiovascular Signs / Tachycardia, rapid pulse, high heart rate Sign
Cardiovascular Signs / Weak pulse, small pulse Sign
Digestive Signs / Diarrhoea Sign
General Signs / Ataxia, incoordination, staggering, falling Sign
General Signs / Dysmetria, hypermetria, hypometria Sign
General Signs / Fever, pyrexia, hyperthermia Sign
General Signs / Generalized lameness or stiffness, limping Sign
General Signs / Lymphadenopathy, swelling, mass or enlarged lymph nodes Sign
General Signs / Pale mucous membranes or skin, anemia Sign
General Signs / Weight loss Sign
Nervous Signs / Dullness, depression, lethargy, depressed, lethargic, listless Sign
Reproductive Signs / Abortion or weak newborns, stillbirth Sign
Respiratory Signs / Coughing, coughs Sign
Respiratory Signs / Dyspnea, difficult, open mouth breathing, grunt, gasping Sign
Respiratory Signs / Increased respiratory rate, polypnea, tachypnea, hyperpnea Sign
Respiratory Signs / Mucoid nasal discharge, serous, watery Sign
Respiratory Signs / Purulent nasal discharge Sign
Skin / Integumentary Signs / Parasite visible, skin, hair, feathers Sign
Skin / Integumentary Signs / Skin edema Sign

Disease Course

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Infections in humans

The clinical presentations of tularaemia in humans are reviewed by Sjöstedt, 2007. Tularaemia normally presents after an incubation period of 3-5 days, with nonspecific symptoms such as fever, malaise, chills, and headache. If the infection is transmitted through the skin or mucous membranes, ulceroglandular tularaemia will result. A primary ulcer usually develops at the site of infection; often patients do not recognize the initial ulcer and it may heal within a week. The lymph nodes draining the ulcer enlarge and become palpable and tender. Without administration of antibiotics within 7-10 days, the enlargement of the lymph nodes continues and suppuration may occur. The ulceroglandular form comprises more than 90% of the European tularaemia cases. It is the predominant form of tularaemia caused by F. tularensis subsp. holarctica but infection by all subspecies may present as ulceroglandular tularaemia.

Respiratory tularaemia results from inhalation of F. tularensis. Farmers appear to be at risk to contract this form from work with contaminated hay (Syrjälä et al., 1985) but also other activities such as lawn-mowing may occasionally give rise to the disease. Outbreaks of this form rarely occur but can affect a considerable number of individuals. The contaminated aerosols most likely result from animal carcasses or excretions from infected animals. Normally the disease is systemic, presenting with fever, but may lack respiratory symptoms and also diagnostic X-ray findings. The outcome of respiratory tularaemia depends on the aetiological agent; infection with F. tularensis subsp. holarctica results in a nonfatal respiratory infection, whereas inhalation of bacteria of subspecies tularensis gives an acute, serious infection characterized by high fever, malaise, chills, and cough and sometimes delirium and pulse-temperature dissociation. The latter form is potentially life-threatening and, historically, had a case-fatality rate of >50%, before effective treatment was available.

Other, uncommon forms of tularaemia include direct inoculation of the eye resulting in oculoglandular tularaemia. The patient usually presents with unilateral conjunctivitis, prominent swelling of the eyelids, photophobia, and a purulent secretion. Another uncommon form, oropharyngeal tularaemia, is the result of ingestion of contaminated water or food. Typhoidal tularaemia is used to describe tularaemia patients with severe systemic symptoms but without any obvious signs of the port of entry.

Infections in animals

In animals, the full spectrum of clinical signs is not known, but syndromes corresponding to the typhoidal, respiratory, ulceroglandular and oropharyngeal forms have been reported. There are only a few reports of the pathology and clinical presentation in wild animals, mostly in lagomorphs (Park et al., 2009; Gyuranecz et al., 2010a).

In susceptible species, such as lagomorphs and rodents, clinical signs of severe depression are often followed by a fatal septicaemia. The course of the disease is approximately 2-10 days, and animals are usually dead when presented for diagnosis.

Several small rodent species are considered very sensitive to F. tularensis; experimental infection of the common hamster (Cricetus cricetus) leads to septicaemic disease and death (Gyuranecz et al., 2010b). Experimentally infected lagomorphs, have been considered to be very sensitive and develop acute disease. In Europe this has been shown in experimentally and naturally infected hares with F. tularensis subsp. holarctica (Borg et al., 1969; Mörner et al., 1988; Decors et al., 2011). However, studies of naturally infected European brown hares (Lepus europaeus) have also described chronic disease (Gyuranecz et al., 2010a), which suggests that the disease in hares does not always have an acute and fatal presentation.

Most domestic species do not usually manifest signs of tularaemia, but they do develop specific antibodies to the organism following infection.

Epizootics of tularaemia were once common among range sheep in Idaho, Montana and Wyoming, and occasional outbreaks can still occur (Philip and Williams, 1985; O’Toole et al., 2008). Outbreaks in sheep are usually characterized by late term abortions in ewes, and illness and deaths among lambs. Fever, listlessness, regional lymphadenopathy and diarrhoea may be seen. Mortality rates up to 10-15% are seen in untreated lambs, but adult sheep do not usually develop systemic signs.

There is seroevidence of natural infection in cattle, but tularaemia has been diagnosed only rarely in sick calves (Philip and Williams, 1985). Experimental infection of calves with F. tularensis induced disease characterized by fever, weakness and inappetance with spontaneous regression of the symptoms (Mardari et al., 1976).

A mare and 5 foals were reported to have developed tularaemia, 2 of which died from the disease. The infected horses were febrile and dyspneic, had signs of depression and incoordination, and were infested with ticks; 1 of the 2 foals that died had no signs of illness. Seroconversion in surviving horses was detected, and F tularensis was isolated from tissues collected at necropsy (Claus et al., 1959). Livestock may be more important as maintenance hosts of the tick vectors rather than as reservoirs of infection.

Cats seem to be relatively susceptible to tularaemia. Sick cats often have severe clinical signs, and the mortality rate is high if the disease is not treated early (Baldwin et al., 1991; Gliatto et al., 1994). However, milder cases are reported occasionally, and some cats with no history of disease are seropositive (Magnarelli et al., 2007).

In cats, infections often begin with the sudden onset of fever, lethargy, anorexia, and regional or generalized lymphadenopathy. The lymph nodes may suppurate and drain. The submandibular lymph nodes are often affected, and oral lesions including white patches or ulcers may be found. Pneumonia, icterus, hepatomegaly, splenomegaly, weight loss and vomiting have also been reported.

Dogs appear to be relatively resistant and may recover spontaneously (Nordstoga et al., 2014). Clinical signs that have been reported in dogs include anorexia, depression, mild fever, lymphadenopathy, draining abscesses, and mucoid ocular discharge or conjunctivitis (Johnson, 1944; Gustafson and DeBowes, 1996; Nordstoga et al., 2014).

In an outbreak among captive prairie dogs, which probably spread by cannibalism, all of the animals had signs of the oropharyngeal form (Petersen et al., 2004). The clinical signs included emaciation, dehydration and lethargy.

Epidemiology

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Tularaemia ecology is not fully understood, with many knowledge gaps about the disease reservoirs and vectors. The extremely broad range of F. tularensis has made the identification of specific ecological transmission cycles challenging (Keim et al., 2007; Sjöstedt, 2007).

Francisella tularensis is adapted to a wide array of arthropod vectors including ticks, flies and mosquitoes. Arthropod transmission of tularaemia occurs throughout the Northern Hemisphere (reviewed by Sjöstedt, 2007; Petersen et al., 2009). The tick is largely believed to be a biological vector of F. tularensis; transmission by mosquitoes and flies is largely believed to be mechanical on the mouthpart through interrupted feedings (Akimana and Kwaik, 2011).

Three tick species and one fly species are widely recognized as the most important vectors of tularaemia to humans in North America. In the south, central, and eastern United States tularaemia transmission is mainly from the ixodid ticks Amblyomma americanum and Dermacentor variabilis, whereas D. andersoni and the tabanid fly Chrysops discalis are thought to be largely responsible for transmitting the disease in the western United States (reviewed by Keim et al., 2007).

In Japan, the ticks Haemaphysalis flava and Ixodes spp. are important vectors (Ohara et al., 1998).

During human outbreaks in northern Europe, including Sweden and Finland, there is an association of tularaemia with mosquito bites (Rydén et al., 2012; Rossow et al., 2014). In central Europe, the ticks Dermacentor reticulatus and Ixodes ricinus are important vectors (Hubálek and Halouzka, 1997; Gurycová et al., 2001; Ellis et al., 2002).

The main components of regional disease cycles typically involve one to a few, key mammalian and arthropod species. Two disease cycles, terrestrial and aquatic, have been described. In the terrestrial cycle, rabbits and hares typically serve as amplifying hosts and ticks or biting flies are arthropod vectors. In the aquatic cycle, beaver, muskrat and voles serve as important mammalian hosts and appear to shed live organisms into their environments (Petersen and Schriefer, 2005). In Sweden, mosquitoes have been strongly implicated as vectors of tularaemia (Rydén et al., 2012; Thelaus et al., 2014) and may acquire infection from other components of the aquatic cycle. It has been suggested that the bacterium persists in watercourses in association with amoebae (Berdal et al., 1996).

F. tularensis can be transmitted by ingestion, inhalation, arthropod-borne transfer, or direct contact with mucous membranes and broken skin (reviewed by Ellis et al., 2002). The most common mode of transmission to humans is via arthropod vectors; however, F. tularensis can be acquired from various sources including lakes and streams, contaminated food, laboratory cultures or clinical samples, and tissues from infected animals. In some regions, hunting or skinning animals, or contact with meat when preparing food, are important routes of exposure (Maurin et al., 2011; Gyuranecz et al., 2012; Otto et al., 2015). Respiratory infections sometimes occur in farmers who are exposed through activities such as piling hay (Syrjälä et al., 1985). Human infections following bites from infected animals have also been reported (Magee et al., 1989; Capellan and Fong, 1993; Friedl et al., 2005; Weinberg and Branda, 2010). Person-to-person transmission has not been reported.

Zoonoses and Food Safety

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Tularaemia is a zoonotic disease. Due to a widespread association with animals and the environment, there are numerous diverse modes of transmission for F. tularensis. These include direct contact with infected mammals (e.g. skinning infected lagomorphs), bites of infectious arthropods, ingestion of contaminated water or food (e.g. raw milk and undercooked meat), inhalation of contaminated aerosols or dust, and bites from infected animals (Ellis et al., 2002; Keim et al., 2007).

Tularaemia is an occupational risk for farmers, hunters, butchers, forestry workers, veterinarians and laboratory workers (Preiksatis et al., 1979, Syrjälä et al., 1985, Deutz et al., 2003; Rusnak et al., 2004; Esmaeili et al., 2014; Richard and Oppliger, 2015).

Human cases have been associated with contact with pet cats (Liles and Burger, 1993; Larson et al., 2014), prairie dogs (Avashia et al., 2004) and sheep (Jellison and Coles, 1955; Senol et al., 1999) as well as wild animals (Maurin et al., 2011; Otto et al., 2015). Tularaemia has been transmitted to people in bites from cats (Capellan and Fong, 1993; Blackburn et al., 2013), a dormouse (Friedl et al., 2005), a ringtail possum (Jackson et al., 2012) and a pet squirrel (Magee et al., 1989), as well as through a scratch by a buzzard (Padeshki et al., 2010).

Disease Treatment

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Tularaemia can be treated with various antibiotics including tetracyclines and quinolones.

In humans with severe tularaemia, parenteral administration of an aminoglycoside is the first choice for treatment. Gentamicin is preferred; streptomycin is an alternative. In less severe cases or in a mass casualty setting, oral ciprofloxacin or doxycycline is preferred. For dosage, see: WHO guidelines on Tularemia, 2007 (pdf).

Prevention and Control

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Vaccines are not available for any animal species. Live attenuated vaccines are occasionally made available to humans at high risk of exposure to virulent F. tularenesis, such as laboratory workers (Ellis et al., 2002; Sjöstedt, 2007). Research is ongoing to develop an improved, fully protective live attenuated vaccine (reviewed by Marohn and Barry, 2013).

In areas where tularaemia is endemic, the handling of dead or moribund wild animals is not recommended, ingestion of uncooked wild game and untreated water sources should be avoided, and the possibility of insect bites should be reduced (Ellis et al., 2002).

Tick control programmes may reduce the risk of infection in livestock. Cats and dogs should be kept from hunting rodents and rabbits in areas where tularaemia is endemic; acaricide application in residential backyards has also been proposed as a preventative measure (Raghavan et al., 2013). Tularaemia is less likely to occur in domesticated rabbits and pet rodents that are housed inside.

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