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#Bacteriologie #Bacteriology #Clinical #Clinique #MDB-Tularemia #MDB-Tularemie #Maladies-infectieuses-et-tropicales #Tularemia
Tularemia is widely distributed, but it is primarily a disease of the Northern Hemisphere, and is most common between 30° and 71° north latitudes.
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It has been remarkably absent from the United Kingdom, Ireland, and South America
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Reports of increased incidence in Europe, including Austria, Norway, Sweden, and Spain, have been ascribed to climate change.80,81,82,83
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Tularemia was very common in the United States before World War II. However, its incidence has declined steadily since the 1950s and has remained at fewer than 0.15 cases per 100,000 population since 1965.85,86
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Because of its stable and low incidence, tularemia was removed from the list of nationally reportable diseases in 1995 but was added back in 2000 in part because of the concern about its use for bioterrorism.
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Since 2001, the case rates have been 0.05 per 100,000 population or less.86
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Groups with high incidence rates include Native Americans and Alaskan Natives
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The southern border of tularemia has shifted northward so that fewer cases have been reported from south central states in recent years.
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Environmental data also have been used to develop a model to predict risk for tularemia in specific geographic regions.89 Detailed investigation using molecular typing found that specific F. tularensis strains may be geographically limited, with strain variation yielding differences in virulence and disease severity.39
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Genotype A1b isolates were significantly more likely from invasive infections associated with significantly higher mortality in humans than A1a and A2 isolates.92
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The distribution of group A1 isolates correlated with the distribution of Amblyomma americanum and Dermacentor variabilis ticks and the eastern cottontail rabbit (Sylvilagus floridanus).91 The distribution of group A2 isolates correlated with the distribution of D. andersoni and the deer fly Chrysops discalis and also with the mountain cottontail rabbit (Sylvilagus nuttalii). There were only a few isolates of F. tu laren si s subsp. novicida, but most were seen in the southeastern United States.90
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Cases of F. t ul a re n s i s subsp. novicida are uncommon. Almost avirulent in normal human hosts, these infections do not resemble customary tularemia, often are bacteremic, and appear to usually occur in patients with immunosuppression or significant comorbidities.23,96
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F. tularensis subsp. mediasiatica is among the least studied, found initially only in sparsely populated regions of Central Asia but more recently described in the Altai region of Russia.25
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Historically, the incidence of tularemia in the United States has been most frequent in June through August as well as December. The summer peak corresponds to a higher number of tick-acquired cases, whereas the smaller peak in winter reflects an increased number of hunting- associated cases.
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A review of 316 available F. tularensis human isolates from 39 states collected between 1964 and 2004 found that 208 (66%) were F. tu la re nsi s subsp. tularensis and 108 (34%) were F. tularensis subsp. holarctica.98 Most isolates of both subspecies occurred between May and September; a very small increase in numbers in December was noted only for F. tu l ar ensi s subsp. tularensis and not for F. t ul aren si s subsp. holarctica, and only F. tu l ar en si s subsp. tularensis was associated with lagomorph exposure.98
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However, in recent years the number of reported infections only peaks in the late spring and summer.97
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In the United States, the number of reported cases are highest in children ages 5 to 9 years and in adult men ages 55 to 59 years (see Fig. 227.2).5,85,86,99
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Occupations that have been associated with an increased risk for tularemia are laboratory worker, farmer, landscaper, veterinarian, sheep worker, hunter or trapper, cook, and meat handler
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In Europe, where most cases are from type B strains, the source and clinical presentation vary by country. Ticks and other insect bites predominate, causing ulceroglandular and glandular tularemia.83
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Oropharyngeal tularemia has caused outbreaks in places with unsafe food and water,100–102 and during wartime, such as in Kosovo.103
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Pneu- monic and typhoidal tularemia are uncommon in Europe.82
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F. tularensis is capable of infecting hundreds of different vertebrates and invertebrates, but no more than a dozen mammalian species are important to its ecology in any geographic region. These include lagomorphs, particularly Sylvilagus and Lepus spp., and rodents such as voles, squirrels, muskrats, and beavers in North America.
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In Eurasia, infected animals include voles, hamsters, mice, and hares.
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of F. tularensis to humans occurs most often through the bite of an insect or contact with contaminated animal products. Other routes of transmission include aerosol droplets, contact with contaminated water or mud, and animal bites.
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Inoculation from freshwater fishhook injury has been described.104
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Illness may occur in families or friends because of shared activities and exposures. Nonetheless, human-to-human spread does not occur
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Blood-feeding arthropods and flies are the most important vectors for tularemia in the United States.
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In contrast, mosquitoes are the most frequent insect vector in Sweden and Finland, and they are also important in the former Soviet Union.
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The dog tick (D. variabilis), wood tick (D. andersoni), and Lone Star tick (A. americanum) are commonly involved in North America.
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The organism may be present in tick saliva or feces inoculated either directly or indirectly into the bite wound
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Tick transmission traditionally has been associated with F. tularensis subsp. tularensis. Several outbreaks of tick-borne tularemia have involved F. tularensis subsp. holarctica, although this organism is more often linked to water, rodents, and aquatic animals.
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Animal contact is another important mode of acquiring tularemia. Skinning, dressing, and eating infected, undercooked animals, including rabbits, muskrats, beavers, squirrels, and birds, has transmitted tularemia, occasionally resulting in large outbreaks in hunters.
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An outbreak in 2000 of pneumonic tularemia on Martha’s Vineyard was associated with mowing lawns and using a brush cutter, likely aerosolizing infected animal carcasses. Since then, cases of pneumonic tularemia have been regularly encountered on Martha’s Vineyard during most summers.109,110 An alternative explanation for pneumonic cases may rest with the finding of large numbers of F. tularensis bacteria within infected ticks, which may suggest that aerosolized ticks rather than animals may also contribute to cases.91
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Domestic cats and other carnivorous animals may carry F. tularensis in the mouth or on claws after killing or feeding on infected prey, whether or not they are infected.112 This is thought to be the mechanism by which occasionally domestic cats, and in one case a buzzard, transmit tularemia.112,113
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F. tularensis may survive for prolonged periods in water, mud, and animal carcasses even if frozen; however, cooking game meats thoroughly to the proper temperatures should minimize risk from ingestion. Nonetheless, contaminated food and water continue to be important environmental sources of tularemia
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Fresh crushed grapes were linked to an outbreak of oropharyngeal tularemia in Germany, probably contaminated with an infected rodent collected by a mechanical harvester.116
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Disruptions of infrastructure caused by wars and natural disasters may also be significant contributing factors. In postwar Kosovo, an epizootic increased rodent population contaminated ransacked homes and food with F. tularensis that led to foodborne and waterborne outbreaks among refugees returning to disrupted housing and sanita- tion.117,118
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It has been demonstrated that F. tularensis subsp. tularensis, F. tularensis subsp. novicida, the live vaccine strain, and F. philomiragia will multiply intracellularly in Acanthamoeba castellanii and infect amebal cysts; F. tularensis subsp. tularensis is capable of surviving in amebal cysts for up to 21 days.29,121,122 Such a relationship may prove relevant to natural aquatic reservoirs for Francisella
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Although the organism is reported to penetrate intact skin, most investigators believe that penetration occurs through sites of skin disruption that may be inapparent if without known cause.
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Organisms may remain viable in carcasses or dust for up to 136 days, and culturable organisms have remained within infected frozen rabbit meat for more than 3 years.123
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The infectious dose in humans depends on the portal of entry: 10 to 50 organisms are sufficient when injected intradermally or when inhaled, though 106 to 108 organisms are required when ingested.123
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In general, F. tularensis subsp. tularensis causes more severe disease than either F. tularensis subsp. holarctica or F. tularensis subsp. novicida. The specific molecular reasons underlying these differences in virulence are unclear.
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During the first 3 to 5 days after cutaneous inoculation, F. tularen si s multiplies locally and produces a papule; ulceration may begin 2 to 4 days later.4 Organisms spread from the site of entry to regional lymph nodes and may disseminate via a lymphohematogenous route to involve multiple organs. Bacteremia is probably common in this early phase, although it is only occasionally detected. Changes in draining regional lymph nodes appear after skin lesions develop.4 An elegant description of the pathogenesis is offered by Geyer and colleagues.124
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Granulomas develop that occasionally may caseate; for this reason, specimens may be mistaken for tuberculosis. These changes can occur in any infected site and have been found at autopsy in lung, liver, spleen, lymph nodes, and bone marrow.
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F. tul are nsi s is contained within granulomas in the livers of mice infected with the vaccine strain, and granuloma formation involves hepatic natural killer cells, interferon-γ (IFN-γ) production, and expression of inducible nitric oxide synthase.125
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The organisms are usually present at the site of the necrotic tissue but are difficult to demonstrate on routine stains. Silver impregnation techniques (Steiner, Dieterle, and Warthin-Starry silver stains) enhance the visibility of the organisms, usually found in macrophages and epi- thelioid cells
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F. tularen si s also can infect erythrocytes and persist within them, where they are protected from killing by gentamicin; this has been proposed as one reason why tularemia may relapse.127 Intraerythrocytic F. t ul a re n si s also are protected from the acidic pH within the tick gut, and this enhances tick colonization.128
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Most organisms recovered from blood in a mouse model of F. tularensis infection were free in plasma and not in leukocytes.126 The organisms grew well in whole blood but not in plasma, implying a requirement for host cells. These observations suggest that circulating F. tularensis may be taken up by leukocytes where they survive and are protected from innate humoral defenses and potentially antibiotic effects, then escape into the plasma where they can begin a cycle of reinfection
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F. tularensis is a facultative intracellular pathogen that is capable of growing within several different cell types, including macrophages, dendritic cells, hepatocytes, alveolar epithelial cells, and endothelial cells.129,130 However, macrophages are the primary site of survival and replication.
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Complement receptors, mannose receptors, class A scavenger receptors, Fcγ receptors, and surface nucleolin may be utilized for F. tu l ar e ns i s uptake, and the specific receptor pathway used may affect early suppression of innate defenses and intracellular trafficking of the organism.129,132,133
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Inside the macrophage, virulent F. tularensis strains impair maturation of the endosome, thus avoiding phagosome-lysosome fusion. Phagosomes containing virulent F. t u la r en s i s are transiently acidified by the vacuolar adenosine triphosphatase pump, and organisms quickly escape into the cytosol. Bacteria proliferate in the cytoplasm, induce apoptotic cell death, and are released to further spread the infection.134
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Neutrophils and macrophages surround earlier inflammatory cells, stimulated by the initial inoculum, that haves become necrotic and degenerated. Eventually, lymphocytes, epithelioid cells, and giant cells migrate into the necrotic tissue. This extensive necrosis is noted in both lung tissue and lymph nodes. As the necrotic tissue expands, adjacent veins and arteries may thrombose.
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Complete recovery from tularemia requires cell-mediated immunity, demonstrable approximately 1 week earlier than antibody responses and directed against protein antigens. This cell-mediated immunity is αβ T-cell dependent but may involve either CD4+ or CD8+ T cells
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Furthermore, different routes of infection and different mouse strains may elicit dissimilar murine immune responses.139
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Humoral immunity, directed against carbohydrate antigens, develops between the second and third weeks after infection, with the almost simultaneous appearance of IgM, immunoglobulin G (IgG), and immunoglobulin A (IgA) agglutinating antibodies. However, antibodies alone are insufficient to protect against virulent F. tularen si s infection.135
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Early host defense against F. tularensi s infection involves neutrophils, dendritic cells, macrophages, mast cells, TNF-α, IFN-γ, and interleukin-12, but these are not sufficient to resolve the infection
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The initial response to F. t ul are ns i s infection is dependent on membrane-associated TLR2 recognition, particularly in the lung, and cytosolic nucleotide oligomerization domain–like receptors.139
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TLR4 recognition of F. tul aren si s LPS is poor; interestingly, the resistance of mice to pulmonary infection with F. tularensis subsp. novicida is enhanced by pretreatment with a TLR4 agonist.146
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The contribution of αβ+ T cells involves TNF-α and IFN-γ production and is dependent on interleukin-12.139 Also, it has been appreciated that both humoral and cellular immune mechanisms act together to achieve protective immunity.148,149
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It survives extracellularly in part because it is capable of avoiding complement- mediated lysis. It survives intracellularly by multiple mechanisms, including prevention of phagosome-lysosome fusion, escape from the phagosome, suppression of the inflammasome, alternative activation of macrophages, avoiding killing by cellular antimicrobial peptides, destabilization of host cell messenger RNA, impairment of proinflam- matory cytokine production, inhibition of NADPH oxidase in neutrophils, and the induction of prostaglandin E2 secretion, which can inhibit IFN-γ production.137,151,152–156 It also is capable of inhibiting IFN-γ signaling and production. For example, impaired clearance of F. tularensis live vaccine strain from mice with pulmonary infection may result from increased local prostaglandin E2 secretion and decreased numbers of IFN-γ–secreting T cells.
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Similarly, lymphocyte responsiveness to the live vaccine strain persists for up to 34 years after vaccination, and IFN-γ expression involves both CD4+ and CD8+ cell populations.150
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The clinical consequences of F. tul ar en si s infection depend on the viru- lence of the particular organism, the portal of entry, the extent of systemic involvement, and the immune status of the host. The result can range from asymptomatic or inconsequential illness to acute sepsis and rapid death.
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Patients who seek medical attention usually present with at least one of six classic forms of tularemia: ulceroglandular, glandular, ocu- loglandular, pharyngeal, typhoidal, and pneumonic. This somewhat artificial classification emphasizes only the predominant manifestations commonly encountered, and overlapping forms may be present in many patients
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The incubation period averages 3 to 5 days, but it ranges from 1 to 21 days.
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Tularemia usually starts abruptly, with the onset of fever that can range to 104°F, chills, headache, malaise, anorexia, and fatigue. Other prominent symptoms may include cough, myalgias, chest dis- comfort, vomiting, sore throat, abdominal pain, and diarrhea.
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A pulse-temperature deficit was noted in up to 42% of evaluable patients in the United States, although this was found in only 5% of patients infected with F. tularensis subsp. holarctica infection in Sweden.159,160
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Fever (usually >38.3°C [101°F]) classically lasts for several days, remits for a short interval, and then recurs along with other symptoms. Without treatment, fever lasts an average of 32 days while chronic debility, weight loss, and lymphadenopathy may persist for many months longer.161
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Less virulent strains cause a milder, self-limited illness that may resolve without therapy.
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Systemic symptoms may abate by the time medical help is sought so that the clinical picture is dominated by one or more of the six patterns listed; this may lead to confusion regarding the correct diagnosis, particularly in the 25% to 50% of patients without an evident source of infection.
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Ulceroglandular and Glandular Tularemia
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Tick bites and animal contacts are the usually recalled exposures.
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Ulceroglandular and Glandular Tularemia
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The initial specific complaint is often of enlarged and tender localized lymphadenopathy (Fig. 227.3)
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Ulceroglandular and Glandular Tularemia
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This form is most quickly recognized as tularemia compared to others.
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Ulceroglandular and Glandular Tularemia
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The inciting skin lesion may appear before, simultaneously with, or from one to several days after the adenopathy. It starts as a red, painful papule in a region draining into the involved lymph nodes. Vesicles also may be seen, and these may be mistaken for herpes simplex or varicella infection.162 The papule then undergoes necrosis, leaving a tender ulcer with a raised border (see Fig. 227.3). If untreated, the ulcer may take weeks to heal and leave a residual scar. Multiple lesions may occur, particularly in those cases with animal sources.160
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Ulceroglandular and Glandular Tularemia
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The location of the ulcer usually reflects the mode of acquisition; animal contacts tend to yield ulcers on the hands and forearms, while tick bites cause ulcers on the trunk, the perineum, the lower extremities, and the head and neck (see Fig. 227.3).
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The distribution of lymph- adenopathy also reflects the exposure history, as illustrated in Fig. 227.4. Overall, cervical and occipital adenopathy are most common in children and inguinal adenopathy is most common in adults.
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Skin changes over the involved nodes occurred in 19.1% of patients in a series from Sweden,159 which suggests underlying suppuration. Some patients have a sporotrichoid presentation with ascending subcutaneous nodules (see Fig. 227.3). Lymphangitis is rare unless there is another bacterial superinfection of the ulcer
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Glandular tularemia occurs when patients present with tender regional lymphadenopathy but without a visible cutaneous lesion. This form has traditionally accounted for one-fifth or fewer of cases in the United States. However, glandular tularemia was the most common primary clinical form in children (44%) and the second most common presenta- tion overall among classifiable cases reported in Missouri between 2000 and 2007.163
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Glandular tularemia represents essentially the same process as ulceroglandular disease, except that a skin lesion either healed before presentation or was minimal, atypical, or overlooked
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Enlarged lymph nodes may persist for prolonged periods. In some patients, an exposure or prior febrile illness will be forgotten. For this reason, tularemia may not be considered in the initial differential diagnosis of some patients whose primary presentation is lymph- adenopathy
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In either ulceroglandular or glandular tularemia, the lymph nodes may suppurate (see Fig. 227.3). More than 20% will suppurate if left untreated or if treatment is delayed longer than 2 weeks.3,164 When fluctuant, they should be needle aspirated or surgically drained.
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The differential diagnosis of ulceroglandular and glandular tularemia includes pyogenic bacterial infections, cat-scratch disease, syphilis, chancroid, lymphogranuloma venereum, tuberculosis, nontuberculous mycobacterial infection, toxoplasmosis, sporotrichosis, Spirillum minus rat-bite fever, anthrax, plague, and herpes simplex virus infection
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Oculoglandular tularemia represents only a minority of cases. In this form, organisms have gained entry through the conjunctiva, from contaminated fingers, splashes, or aerosols. The disease may be bilateral, but this is uncommon.
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Early complaints may include photophobia and excessive lacrimation.
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Examination shows lid edema and painful conjunctivitis, with injection, chemosis, and small, yellowish conjunctival ulcers or papules in some patients. Associated tender lymphadenopathy may occur in the preauricular, postauricular, submandibular, and cervical regions. If the adenopathy is extensive and more prominent than the eye findings, then this syndrome may be mistaken for mumps.160
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Visual loss is rare, but complications include corneal ulceration, dacryocystitis, and nodal suppuration. Other ocular manifestations of tularemia also have been described, including cases of uveitis.165,166
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The differential diagnosis of oculoglandular tularemia includes pyogenic bacterial infections, adenoviral infection, syphilis, cat-scratch disease, and herpes simplex virus infection
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Tularemia may be an overlooked cause of Parinaud oculoglandular syndrome (conjunctivitis with ipsilateral preauricular adenopathy).167
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Pharyngeal tularemia, another variant of ulceroglandular disease, is the result of primary invasion through the oropharynx. The source may be contaminated food, water, or droplets.
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This form represents few cases overall in the United States, though it has been increasingly described in other countries with outbreaks.168–170 In a large retrospective series from Turkey, pharyngeal tularemia accounted for 85% of cases.168 Children appear to acquire this form more often than adults, and several family members may be affected simultaneously, especially if drinking from contaminated wells or other unchlorinated water sources.102,168
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Pharyngeal Tularemia
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This form must be distinguished from a sore throat that may accompany any of the other major clinical forms of tularemia. In pharyngeal tularemia, the predominant complaints are fever, severe throat pain, and a neck mass representing lymphadenopathy. Exudative pharyngitis or tonsillitis is the rule, and one or more ulcers may be seen.
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Pharyngeal Tularemia
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A pharyngeal membrane has been described in some patients that is similar to a diphtheritic membrane.161 Cervical, pre-parotid, and retropharyngeal adenopathy may be present, occasionally with bilateral involvement or abscess formation.
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Pharyngeal Tularemia
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When there is a delay in seeking care, the dominant manifestation may be cervical adenopathy without prominent fever or pharyngotonsillitis
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Pharyngeal Tularemia
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The differential diagnosis includes streptococcal pharyngitis, infectious mononucleosis, adenoviral infection, diphtheria, and tuberculosis; the latter especially may be confused with tularemia when granulomatous lymphadenitis is identified on biopsy.171
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Pharyngeal Tularemia
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Tularemia should be suspected in an endemic area whenever a severe sore throat is unresponsive to penicillin therapy and routine diagnostic tests have been unrewarding
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