Epidemiologic and molecular analysis of human tularemia, United States, 1964-2004.Tularemia tularemia (t  lərē`mēə) or rabbit fever, acute, infectious disease caused by Francisella tularensis (Pasteurella tularensis). in the United States is caused by 2 subspecies subspecies, also called race, a genetically distinct geographical subunit of a species. See also classification. of
Francisella tularensis Francisella tu·la·ren·sisn. A bacterium of the genus Francisella that causes tularemia in humans. , subspecies tularensis (type A) and subspecies holarctica (type B). We compared clinical and demographic features of human tularemia cases from 1964 to 2004 from 39 states in which an isolate was recovered and subtyped. Our data indicate that type A and type B infections differ with respect to affected populations, anatomic site of isolation, and geographic distribution. Molecular subtyping with pulsed-field gel electrophoresis further defined 2 subpopulations of type A (type A-east and type A-west) that differ with respect to geographic distribution, disease outcome, and transmission. Our data suggest that type A-west infections are less severe than either type B or type A-east infections. Through a combined epidemiologic and molecular approach to human cases of tularemia, we provide new insights into the disease for future investigation. ********** Tularemia is a zoonotic disease caused by the gram-negative bacterium Francisella tularensis (1). Transmission occurs through arthropod arthropod Any member of the largest phylum, Arthropoda, in the animal kingdom. Arthropoda consists of more than one million known invertebrate species in four subphyla: Uniramia (five classes, including insects), Chelicerata (three classes, including arachnids and horseshoe bites (especially ticks and deerflies), ingestion ingestion /in·ges·tion/ (-chun) the taking of food, drugs, etc., into the body by mouth. in·ges·tion n. 1. The act of taking food and drink into the body by the mouth. 2. of contaminated contaminated, v 1. made radioactive by the addition of small quantities of radioactive material. 2. made contaminated by adding infective or radiographic materials. 3. an infective surface or object. food or water, inhalation of contaminated aerosols, and handling of infected animal tissues. Human illness usually takes 1 of several clinical forms. The most common is ulceroglandular tularemia; more serious forms include pneumonic pneumonic /pneu·mon·ic/ (noo-mon´ik) 1. pulmonary (1). 2. pertaining to pneumonia. pneu·mon·ic adj. 1. Relating to, affected by, or similar to pneumonia. , typhoidal typhoidal /ty·phoid·al/ (ti-foi´dal) resembling typhoid fever. , and meningitic tularemia. Nearly all human cases of tularemia in the United States are caused by F. tularensis subspecies tularensis (type A) or F. tularensis subspecies holarctica, (type B) (2). Type A and B isolates can be differentiated on the basis of glycerol glycerol, glycerin, glycerine, or 1,2,3-propanetriol (prō`pāntrī'ŏl), CH2OHCHOHCH2OH, colorless, odorless, sweet-tasting, syrupy liquid. fermentation, virulence in animal models, and by polymerase chain reaction polymerase chain reaction (pŏl`ĭmərās') (PCR), laboratory process in which a particular DNA segment from a mixture of DNA chains is rapidly replicated, producing a large, readily analyzed sample of a piece of DNA; the process is (3-5). Recently, molecular assays have been developed to further discriminate within subspecies by using pulsed-field gel electrophoresis (PFGE PFGE Pulsed-Field Gel Electrophoresis ), multiple-locus variable-number tandem repeat analysis (MLVA MLVA Micro Light Valve Array MLVA Multi-locus VNTR Analysis MLVA Multiple VNTR Locus Analysis ), whole-genome microarrays, and single nucleotide variations (6-9). In nature, the 2 subspecies are thought to be maintained in distinct but incompletely defined cycles (10-12). Although both subspecies of F. tularensis cause human illness (10), the clinical and epidemiologic features of type A and type B infections have not been systematically compared for a substantial number of cases. Furthermore, the implications of other subgroupings, as defined by molecular techniques, are largely unknown. We identified to subspecies level all human F. tularensis isolates that were submitted to the Centers for Disease Control and Prevention Centers for Disease Control and Prevention (CDC), agency of the U.S. Public Health Service since 1973, with headquarters in Atlanta; it was established in 1946 as the Communicable Disease Center. (CDC See Control Data, century date change and Back Orifice. CDC - Control Data Corporation ) for a 40-year period and further sub-typed a portion by PFGE. Our findings demonstrate distinct subpopulations of F. tularensis that differ in their clinical manifestations, geographic location, and likely modes of transmission. Methods We analyzed all available F. tularensis isolates from humans (n = 316) recovered by or submitted to CDC by state and local health departments from 1964 through 2004. All work with F. tularensis cultures was performed in a biosafety level biosafety level Epidemiology A classification for the degree of caution required when working with specific groups of pathogens. See Maximum containment facility. 3 (BSL-3) laboratory using BSL-3 safety precautions. Isolates were confirmed as F. tularensis by characteristic growth on agar and direct fluorescence antibody staining. Type A and type B isolates were differentiated by biochemical subtyping (glycerol fermentation) with the 96-well automated MicroLog MicroStation System with GN2 Microplates (Biolog Inc, Hayward, CA, USA) (13). Demographic and clinical data on source patients were extracted from submission forms that accompanied the isolates. Extracted information included patient age and sex, date of disease onset, form of clinical disease, anatomic source of isolate, underlying illness, outcome, county where infected, and likely mode of transmission. Isolates received after 1990 (n = 155) were matched with patients reported through the National Electronic Telecommunication Surveillance System to extract county of exposure. Information was verified by contacting the reporting state health department. PFGE subtyping was performed on a subset of isolates with a modified version of the PulseNet 1-day standardized protocol for subtyping foodborne pathogens (14,15). A total of 41 type A and 22 type B isolates were used. DNA-embedded agarose agarose more highly purified form of agar with similar uses to agar and widely used in the separation of nucleic acid fragments. plugs were prepared and lysed under BSL-3 conditions. PFGE plugs were cut (2.0 mm) and digested with 40 U PmeI enzyme (New England Biolabs New England Biolabs (NEB) produces and supplies reagents for the life science industry. NEB offers a large selection of recombinant and native enzymes for genomic research. It also offers products in the areas related to proteomics and drug discovery. , Beverly, MA, USA) for 6 hours at 37[degrees]C under BSL-2 conditions. Salmonella enterica serotype serotype /se·ro·type/ (ser´o-tip) the type of a microorganism determined by its constituent antigens; a taxonomic subdivision based thereon. se·ro·type n. See serovar. v. Braenderup (H9812) was used as a reference standard, and DNA DNA: see nucleic acid. DNA or deoxyribonucleic acid One of two types of nucleic acid (the other is RNA); a complex organic compound found in all living cells and many viruses. It is the chemical substance of genes. plugs were digested with 50 U XbaI enzyme (Roche Diagnostics, Indianapolis, IN, USA) for 3 hours at 37[degrees]C. Seakem agarose gels (1%) were prepared with 0.5x Trisborate-EDTA buffer (Sigma, Saint Louis, MO, USA), and digested DNA plugs were loaded on the comb. Electrophoresis was performed with a CHEF Mapper (Bio-Rad, Hercules, CA, USA) with switch times of 1.79 to 10.71 s at 6V/cm for 17.5 h at 14[degrees]C. Gels were stained with ethidium bromide (1 mg/mL) and gel images captured by using a Gel Doc 1000 imager (Bio-Rad). Analysis of PFGE gels was performed with BioNumerics software version 3.0 (Applied Maths BVBA BVBA Besloten Vennootschap met Beperkte Aansprakelijkheid , Sint-Martens-Latem, Belgium). Gels were normalized by using the Salmonella reference strain. A dendrogram A dendrogram is a tree diagram frequently used to illustrate the arrangement of the clusters produced by a clustering algorithm (see cluster analysis). Dendrograms are often used in computational biology to illustrate the clustering of genes. was constructed with Dice similarity coefficients and unweighted pair group method with averages (UPGMA UPGMA Unweighted Pair Group Method, Arithmetic Mean ). Demographic and clinical data were analyzed with EpiInfo 2002 (CDC, Atlanta, GA, USA). To analyze categorical data categorical data data relating to category such as qualitative data, e.g. dog, cat, female. It may be nominal when a name is used, e.g. location, breed, or ordinal when a range of categories is used, e.g. calf, yearling, cow. and nonparametric tests for continuous data, [chi square chi square (kī), n a nonparametric statistic used with discrete data in the form of frequency count (nominal data) or percentages or proportions that can be reduced to frequencies. ] was used. Results A total of 316 F. tularensis isolates from 39 states were available for analysis; 208 (66%) were type A, and 108 (34%) were type B (Table 1). Among the 10 states submitting at least 10 isolates, the distribution of the 2 subspecies was nonrandom ([chi square] = 34, p <0.0001). Overall, the 2 subspecies segregated into several geographically distinct clusters (Figure 1). Most isolates on the eastern seaboard, in and around Arkansas and Oklahoma, and in the broad area from the Colorado Rockies west to the Sierra Nevada Mountains were type A. In contrast, most isolates from the northern Pacific Coast and along tributaries of the Mississippi River were type B. [FIGURE 1 OMITTED] To further understand this geographic clustering, we developed a PFGE subtyping method for F. tularensis using PmeI. PFGE differentiated both between type A and B strains and among type A strains (Figure 2). Electrophoresis conditions were optimized to resolve restriction fragments between 25 kb and 125 kb for both F. tularensis and the Salmonella reference strain. Reproducibility testing verified that no differences in PFGE patterns were observed between experiments. [FIGURE 2 OMITTED] Comparison of PFGE patterns for a subset of isolates (41 type A, 22 type B) from distinct locations (Figure 3) showed that all 22 type B isolates yielded the same PFGE pattern, which is consistent with previous data showing that type B strains exhibit little genetic diversity (7). In contrast, the type A isolates yielded PFGE patterns that fell into 2 main clusters (Figure 3; 32 type A-east, 9 type A-west). Isolates from 1 cluster came from states completely west of the 100th meridian (type A-west), while the remainder came from states transecting or east of the 100th meridian (type A-east, Figure 1). Based on the PFGE clustering, subsequent epidemiologic analysis was performed separately for type A isolates from the eastern (n = 133; type A-east) and western (n = 71; type A-west) contiguous United States. [FIGURE 3 OMITTED] Information on age and sex was known for 290 (92%) and 312 (99%) source patients, respectively. Males accounted for 75% (157/208) of type A and 72% (75/104) of type B infections. Patients with type A infections were significantly younger than patients with type B infections (median age 38 years vs. 50 years, p<0.01), and patients with type A-west infections were significantly younger than those with type A-east infections (median age 33 years vs. 44 years, p <0.02). An immunocompromising condition (e.g., malignancy, organ transplant, and HIV HIV (Human Immunodeficiency Virus), either of two closely related retroviruses that invade T-helper lymphocytes and are responsible for AIDS. There are two types of HIV: HIV-1 and HIV-2. HIV-1 is responsible for the vast majority of AIDS in the United States. infection) was reported for 11 (10%) of 108 type B-infected patients, 6 (5%) of 133 type A-east-infected patients, and none (0%) of 68 type A-west-infected patients (p<0.01). For the 235 (74%) source patients for whom outcome was known, the overall case-fatality rate was 9% (20/235), with similar rates for infections caused by type A (9%, [15/161]) and type B (7% [5/74]) isolates. However, among type A infections, case-fatality rates differed markedly between type A-east (14% [15/106]) and type A-west (0% [0/55]) (p<0.002). Information on anatomic source was available for 280 (89%) isolates. Overall, more than half of the isolates were recovered from lymph nodes Lymph nodes Small, bean-shaped masses of tissue scattered along the lymphatic system that act as filters and immune monitors, removing fluids, bacteria, or cancer cells that travel through the lymph system. and a quarter from blood (Table 2). While type A and type B isolates did not differ significantly with respect to anatomic source, significant differences were observed between type A-west and both type A-east (p<0.001) and type B (p<0.002) isolates. Type A-east and type B isolates were more likely than type A-west isolates to be recovered from blood and lung (Table 2), whereas type A-west isolates were more likely to be recovered from lymph nodes. The clinical form of the disease was known for only 104 (33%) source patients. Ulceroglandular and glandular glandular /glan·du·lar/ (glan´du-ler) 1. pertaining to or of the nature of a gland. 2. glanular. glan·du·lar adj. 1. were the most commonly reported clinical forms of tularemia, accounting for 68 (65%) of 104 cases with information available. Other clinical syndromes included pneumonic (17%, 18/104), typhoidal (12%, 12/104), oculoglandular (4%, 4/104), meningitic (1%, 1/104) and pharyngeal pharyngeal /pha·ryn·ge·al/ (fah-rin´je-al) pertaining to the pharynx. pha·ryn·geal or pha·ryn·gal adj. Of, relating to, located in, or coming from the pharynx. (1%, 1/104) forms. Patients with typhoidal or pneumonic disease were generally older (median age 48 years and 53 years, respectively) than those with either glandular or ulceroglandular disease (median age 11 years and 37 years, respectively). Among the subset of patients for whom a clinical form of infection was reported, glandular or ulceroglandular disease was diagnosed more frequently in patients with type A infections (71% vs. 52% for type B) and pneumonic disease was diagnosed less frequently (12% vs. 30% for type B). Among 292 source patients whose date of disease onset was known, 210 (72%) were infected in May through September; no difference in onset between type A and B infections was noted (Figure 4). A possible source of infections was reported for 133 (42%) of 316 patients. Direct animal contact accounted for 47 (47%) of 99 type A and 18 (53%) of 34 type B infections. Most type A infections were associated with exposure to either lagomorphs (53%, 25/47) or cats (30%, 14/47). Type B infections were most often associated with exposure to rodents (33%, 6/18) or cats (22%, 4/18); none were linked to lagomorph exposure. Arthropod bites accounted for 44 (44%) type A infections and 10 (29%) type B infections. Although the arthropod involved was not always identified, ticks were reported as the source for 21 (100%) of 21 type A-east, 9 (100%) of 9 type B, and 4 (44%) of 9 type A-west infections. Biting flies were only linked to type A-west infections and accounted for 5 (55%) of 9 type A-west infections attributed to a known arthropod bite. The remaining 8 (8%) type A and 6 (18%) type B infections were in patients with both animal and arthropod exposure or were attributed to environmental exposures such as landscaping. [FIGURE 4 OMITTED] Discussion Categorization of F. tularensis type A and type B was first proposed by Olsufiev et al. in 1959 (16). These 2 subspecies have been suggested to differ in their ecology and possibly their virulence for humans (17). Our study, which includes isolates obtained during a 40-year period, further refines these views. By combining PFGE subtyping of isolates with geographic data, we found evidence that human type A infections can be further divided into at least 2 distinct subgroups (type A-east and type A-west). In addition, our data suggest that type A-west infections are less severe than type B or type A-east infections. The most notable finding of this investigation concerns fatality rates. The case-fatality rate for type A-east infections was 14%, compared with 7% for type B infections and 0% for type A-west infections. Type A-east and type B isolates were more likely to have been recovered from patients' lungs or blood, whereas type A-west isolates were more often isolated from lymph nodes. The apparent reduced invasiveness of type A-west strains may be explained by the younger age of the patients infected. However, a review of the literature shows that few, if any, tularemia deaths have been reported in the Rocky Mountain region The Rocky Mountain Region is a floristic region within the Holarctic Kingdom in western North America (Canada and the United States) delineated by Armen Takhtajan and Robert F. Thorne. (18-21), regardless of patient age. We hypothesize hy·poth·e·size v. hy·poth·e·sized, hy·poth·e·siz·ing, hy·poth·e·siz·es v.tr. To assert as a hypothesis. v.intr. To form a hypothesis. that the milder form of clinical disease associated with type A-west may be due to differences in virulence factors or perhaps infectious doses associated with differing modes of transmission. Infections caused by type A-west, type A-east, and type B appear to occur in distinct geographic foci, suggestive of suggestive of Decision making adjective Referring to a pattern by LM or imaging, that the interpreter associates with a particular–usually malignant lesion. See Aunt Millie approach, Defensive medicine. different ecologic niches. Type B infections cluster along major waterways, such as the upper Mississippi River
The Upper Mississippi River is the portion of the Mississippi River upstream of Cairo, Illinois, United States. , and in areas with high rainfall, such as coastal areas of the Pacific Northwest. Type A-west infections predominate in the arid region from the Rocky Mountains west to the Sierra Nevada Mountains. Type A-east infections occur in 2 main areas: 1) the central southeast states of Arkansas, Missouri, and Oklahoma and 2) along the Atlantic Coast, east of the Appalachians. The central southeast region is a major focus of human tularemia, accounting for 50% of all reported cases in the United States (22). The type A-east infections along the Atlantic Coast may be linked to the importation of rabbits from Arkansas, Oklahoma, Missouri, and Kansas to hunting clubs in Massachusetts, Pennsylvania, New Jersey, and Maryland in the 1920s and 1930s (17,23). Whether the geographic demarcation of type A-west and type A-east adheres strictly with the 100th meridian will require further PFGE analysis of more type A strains. Animal studies have indicated that type A isolates are often associated with lagomorphs (rabbits and hares), while type B isolates are more often obtained from rodents (12,17). Consistent with these findings, our results show that human type A-east and type A-west infections were associated with exposure to lagomorphs, whereas human type B infections were associated with exposure to rodents. Both type A and type B infections were associated with exposure to cats. Ticks were implicated im·pli·cate tr.v. im·pli·cat·ed, im·pli·cat·ing, im·pli·cates 1. To involve or connect intimately or incriminatingly: evidence that implicates others in the plot. 2. in transmission of both type A-east and type B infections to humans, whereas biting flies were only implicated in transmission of type A-west infections. The restriction of deerflies (Chrysops spp.) and associated human cases to western states was previously noted by Jellison (24). This study is subject to several limitations, including record completeness, ascertainment bias, and number of E tularensis isolates PFGE subtyped. Subspecies differentiation for F. tularensis has historically been dependent on the recovery of an isolate, and subtype (programming) subtype - If S is a subtype of T then an expression of type S may be used anywhere that one of type T can and an implicit type conversion will be applied to convert it to type T. information is not captured in the national disease reporting system. The overall case-fatality rate in this study was 9%, which is severalfold sev·er·al·fold adj. 1. Having several parts or members. 2. Being several times as much or as many. sev higher than the <2% previously reported (25). The higher rate suggests enhanced ascertainment of fatal cases. In addition, 36% of type A-east and 25% of type B isolates were recovered from blood, a much higher rate than previously reported. By analyzing only patients with culture-confirmed infections, we may have selected for patients with more fulminant ful·mi·nant adj. Occurring suddenly, rapidly, and with great severity or intensity, usually of pain. ful disease. Our results demonstrate that PmeI PFGE subtyping is useful for dividing type A isolates into geographically and clinically meaningful subgroups. Nineteen type A isolates analyzed by PFGE in this study (12 type A-east, 7 type A-west) were previously analyzed by MLVA and divided into 2 subpopulations, A.I and A.II (26). Subpopulations independently identified by the 2 methods are in complete agreement, which suggests that type A-west is analogous to A.II and type A-east is analogous to A.I. With training and interlaboratory validation, the PFGE method described here could be adopted by PulseNet laboratories throughout the country that use the standardized PulseNet PFGE protocol for foodborne pathogens (27). The PulseNet network is an existing laboratory infrastructure with all of the necessary equipment and software to perform, normalize normalize to convert a set of data by, for example, converting them to logarithms or reciprocals so that their previous non-normal distribution is converted to a normal one. , and compare PFGE patterns. PFGE subtyping of F. tularensis isolates would allow states to determine the potential geographic origins of tularemia cases and also share and compare their PFGE patterns within the PulseNet network. Although type A is often referred to as the more virulent subspecies of F. tularensis and of greatest concern with respect to bioterrorism, our comparative analysis suggests that this view should be reevaluated. We found that human type A-west infections are markedly less severe than type B infections. Further studies are warranted to determine the basis of the clinical, geographic, and ecologic differences between infections caused by type B, type A-west, and type A-east. Acknowledgments We thank all the persons at state and local health departments who aided in obtaining isolates and clarifying information related to the isolates. We also thank Leon Carter, Kiersten Kugeler, Sandy Urich, and Brook Yockey for their assistance in growing F. tularensis isolates and data extraction and the Special Bacteriology bacteriology Study of bacteria. Modern understanding of bacterial forms dates from Ferdinand Cohn's classifications. Other researchers, such as Louis Pasteur, established the connection between bacteria and fermentation and disease. Reference Laboratory, Meningitis and Special Pathogens Branch, CDC, for sharing their archived F. tularensis isolates. References (1.) Ellis J, Oyston CF, Green M, Titball RW. Tularemia. Clin Microbiol Rev. 2002;15:631-46. (2.) Petersen JM, Schriefer ME. Tularemia: emergence/re-emergence. Vet Res. 2005;36:455-67. (3.) Olsufiev NG, Meshcheryakova IS. Infraspecific in·fra·spe·cif·ic adj. Occurring within a species. infraspecific Occurring within a species; intraspecific. taxonomy of tularemia agent Francisella tularensis McCoy et Chapin. J Hyg Epidemiol Microbiol Immunol. 1982;26:291-9. (4.) Jellison WL, Owen C, Bell JF, Kohls GM. Tularemia and animal populations: ecology and epizootiology. Wildlife Disease. 1961; 17:1-22. (5.) Johansson A, Ibrahim A, Goransson I, Eriksson U, Gurycova D, Clarridge JE III, et al. Evaluation of PCR-based methods for discrimination of Francisella species and subspecies and development of a specific PCR PCR polymerase chain reaction. PCR abbr. polymerase chain reaction Polymerase chain reaction (PCR) that distinguishes the two major subspecies of Francisella tularensis. J Clin Microbiol. 2000;38:4180-5. (6.) Garcia Del Blanco N, Dobson ME, Vela vela plural of velum. AI, De La Puente VA, Gutierrez CB, Hadfield TL, et al. Genotyping of Francisella tularensis strains by pulsed-field gel electrophoresis, amplified fragment length polymorphism Amplified fragment length polymorphism PCR, or "AFLP-PCR" (often AFLP), is a tool used in the study of genetics and in the practice of genetic engineering. Amplified Fragment Length Polymorphism (AFLP fingerprinting, and 16S rRNA gene sequencing. J Clin Microbiol. 2002;40:2964-72. (7.) Johansson A, Farlow J, Larsson P, Dukerich M, Chambers E, Bystrom M, et al. Worldwide genetic relationships among Francisella tularensis isolates determined by multiple-locus variable-number tandem repeat analysis. J Bacteriol. 2004;186:5808-18. (8.) Samrakandi MM, Zhang C, Zhang M, Nietfeldt J, Kim J, Iwen PC. Genome diversity among regional populations of Francisella tularensis subspecies tularensis and Francisella tularensis subspecies holarctica isolated from the US. FEMS FEMS Federation of European Microbiological Societies FEMS Federation of European Materials Societies FEMS Fabrication Engineering Management System FEMS Facility Equipment Maintenance System (PMEL/TMDE) Microbiol Lett. 2004;237:9-17. (9.) Svensson K, Larsson P, Johansson D, Bystrom M, Forsman M, Johansson A. Evolution of subpecies of Francisella tularensis. J Bacteriol. 2005; 187:3903-8. (10.) Jellison WL. Tularemia in Montana. Montana Wildlife. 1971. p. 5-24. (11.) Bell JF. Tularemia--a review. CRC (Cyclical Redundancy Checking) An error checking technique used to ensure the accuracy of transmitting digital data. The transmitted messages are divided into predetermined lengths which, used as dividends, are divided by a fixed divisor. handbook series in zoonoses Zoonoses Infections of humans caused by the transmission of disease agents that naturally live in animals. People become infected when they unwittingly intrude into the life cycle of the disease agent and become unnatural hosts. . Boca Raton (FL): CRC Press; 1977. Section A, p. 161. (12.) Hopla CE, Hopla AK. Tularemia. In: Beran GW, Steele JH, editors. Handbook of zoonoses. 2nd ed. Boca Raton (FL): CRC Press, Inc.; 1994. p. 113-26. (13.) Petersen JM, Schriefer M, Carter LG, Zhou Y, Sealy T, Bawiec D, et al. Laboratory analysis of tularemia in wild trapped, commercially distributed prairie dogs, Texas, 2002. Emerg Infect Dis. 2004;10:419-25. (14.) Ribot EM, Fair M, Gautom R, Cameron DN, Hunter SB, Swaminathan B, et al. Standardization of pulsed-field gel electrophoresis protocols for the subtyping of Escherichia coli Escherichia coli (ĕsh'ərĭk`ēə kō`lī), common bacterium that normally inhabits the intestinal tracts of humans and animals, but can cause infection in other parts of the body, especially the urinary tract. O 157:H7, Salmonella, and Shigella shigella Any of the rod-shaped bacteria that make up the genus Shigella, which are normal inhabitants of the human intestinal tract and can cause dysentery, or shigellosis. Shigellae are gram-negative (see gram stain), non-spore-forming, stationary bacteria. S. for PulseNet. Foodborne Pathog Dis. 2006;3:59-67. (15.) Kubota K, Barrett TJ, Ackers ML, Brachman PS, Mintz ED. Analysis of Salmonella serotype Typhi pulsed-field gel electrophoresis patterns associated with international travel. J Clin Microbiol. 2005;43:1205-9.. (16.) Olsufiev NG, Emelyanova OS, Dunaeva TN. Comparative study of strains of B. tularense in the Old and New World and their taxonomy. J Hyg Epidemiol Microbiol Immunol. 1959;3:138-49. (17.) Jellison W. Tularemia in North America, 1930-1974. Missoula (MT): University of Montana; 1974. (18.) Geiger JC, Meyer KF. Tularemia in Nevada. California and Western Medicine. 1929;31:1-4. (19.) Lane R. Ecological and epidemiological studies of tularemia in California. California Vector Views. 1977;24:39-49. (20.) Hillman Hillman was a famous British automobile marque, manufactured by the Rootes Group. It was based in Ryton-on-Dunsmore, near Coventry, England, from 1907 to 1976. Before 1907 the company had built bicycles. CC, Morgan MT. Tularemia: report of a fulminant epidemic transmitted by the deer fly deer fly see chrysops. . JAMA JAMA abbr. Journal of the American Medical Association . 1937;108:538-40. (21.) Klock LE, Olsen PF, Fukushima T. Tularemia epidemic associated with the deerfly. JAMA. 1973;226:149-52. (22.) Centers for Disease Control and Prevention. Tularemia--United States, 1990-2000. MMWR MMWR Morbidity & Mortality Weekly Report Epidemiology A news bulletin published by the CDC, which provides epidemiologic data–eg, statistics on the incidence of AIDS, rabies, rubella, STDs and other communicable diseases, causes of mortality–eg, Morb Mortal Wkly Rep. 2002;51:182-4. (23.) Belding DL, Merrill B. Tularemia in imported rabbits in Massachusetts. N Engl J Med. 1941;224:1085-7. (24.) Jellison W. Tularemia: geographic distribution of "deerfly fever" and the biting fly, Chrysops discalis Williston. Public Health Rep. 1950;65:149-52. (25.) Dennis DT, Inglesby TV, Henderson DA, Bartlett JG, Ascher MS, Eitzen E, et al. Tularemia as a biological weapon: medical and public health management. JAMA. 2001;285:2763-73. (26.) Farlow J, Wagner DM, Dukerich M, Stanley M, Chu M, Kubota K, et al. Francisella tularensis in the United States. Emerg Infect Dis. 2005;11:1835-41. (27.) Swaminathan B, Barrett TJ, Hunter SB, Tauxe RV. CDC PulseNet Task Force. PulseNet: The molecular subtyping network for foodborne bacterial disease surveillance, United States. Emerg Infect Dis. 2001;7:382-9. J. Erin Staples, * ([dagger]) (1) Kristy A. Kubota, * (1) Linda G. Chalcraft, * Paul S. Mead, * and Jeannine M. Petersen * * Centers for Disease Control and Prevention, Fort Collins, Colorado The City of Fort Collins, a home rule municipality situated on the Cache la Poudre River along the Colorado Front Range, is the county seat and most populous city in Larimer County, Colorado. , USA; and ([dagger]) Centers for Disease Control and Prevention, Atlanta, Georgia, USA (1) These authors Contributed equally to this article. Address for correspondence: Jeannine M. Petersen, Centers for Disease Control and Prevention, Division of Vector-Borne Infectious Diseases, Bacterial Zoonoses Branch, PO Box 2087, Fort Collins, CO 80522, USA; email: JPetersen@cdc.gov Dr Staples served as an Epidemic Intelligence Service The Epidemic Intelligence Service is a program of the United States' Centers for Disease Control and Prevention. Established in 1951 due to biological warfare concerns arising from the Korean War, it has become a hands-on two-year postgraduate training program in epidemiology, with officer in the Bacterial Zoonoses Branch, Division of Vector-Borne Infectious Diseases, National Center for Infectious Diseases, CDC, Fort Collins, Colorado, from 2003 to 2005. She is currently a pediatric pediatric /pe·di·at·ric/ (pe?de-at´rik) pertaining to the health of children. pe·di·at·ric adj. Of or relating to pediatrics. infectious disease Infectious disease A pathological condition spread among biological species. Infectious diseases, although varied in their effects, are always associated with viruses, bacteria, fungi, protozoa, multicellular parasites and aberrant proteins known as prions. fellow at Duke University Medical Center in Durham, North Carolina Durham is a city in the U.S. state of North Carolina. It is the county seat of Durham CountyGR6 and is the fourth-largest city in the state by population. .
Table 1. Number of type A and type B Francisella tularensis
isolates, United States, 1964-2004 *
State Type A Type B Total
Alaska 2 0 2
Arizona 4 0 4
Arkansas 16 0 16
California 3 7 10
Colorado 19 8 27
Delaware 3 0 3
Georgia 5 1 6
Idaho 1 2 3
Illinois 2 6 8
Indiana 1 6 7
Iowa 2 1 3
Kansas 9 0 9
Kentucky 3 20 23
Louisiana 7 0 7
Maine 4 0 4
Maryland 5 0 5
Michigan 1 2 3
Minnesota 0 1 1
Mississippi 2 1 3
Missouri 12 8 20
Montana 0 1 1
Nebraska 6 1 7
Nevada 9 0 9
New Jersey 1 0 1
New Mexico 6 0 6
New York 5 3 8
North Carolina 4 0 4
North Dakota 3 5 8
Ohio 1 1 2
Oklahoma 14 1 15
Oregon 8 14 22
Pennsylvania 1 0 1
South Dakota 9 4 13
Tennessee 4 0 4
Texas 4 1 5
Utah 8 0 8
Virginia 9 1 10
Washington 0 8 8
Wyoming 13 3 16
Unknown 2 2 4
Total 208 108 316
* Submitted to the Centers for Disease Control and Prevention.
Table 2. Anatomic source of Francisella tularensis isolates,
United States, 1964-2004
Type Type
Type A, Type B, A-east, A-west,
Site no. (%) * no. (%) no. (%) no. (%)
Blood 46 (25) 24 (24) 43 (36) 3 (5)
Cerebrospinal fluid 5 (3) 0 (0) 4 (3) 1 (2)
Eye 2 (1) 5 (5) 1 (1) 1 (2)
Lung 18 (10) 12 (12) 14 (12) 3 (5)
Lymph node 109 (60) 58 (59) 56 (48) 53 (87)
* One additional isolate was recovered from a penial exudate.
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