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1.  Incidence of Rocky Mountain spotted fever among American Indians in Oklahoma. 
Public Health Reports  2000;115(5):469-475.
OBJECTIVE: Although the state of Oklahoma has traditionally reported very high incidence rates of Rocky Mountain spotted fever (RMSF) cases, the incidence of RMSF among the American Indian population of the state has not been studied. The authors used data from several sources to estimate the incidence of RMSF among American Indians in Oklahoma. METHODS: The authors retrospectively reviewed an Indian Health Service (IHS) hospital discharge database for 1980-1996 and available medical charts from four IHS hospitals. The authors also reviewed RMSF case report forms submitted to the Centers for Disease Control and Prevention (CDC) for 1981-1996. RESULTS: The study data show that American Indians in the IHS Oklahoma City Area were hospitalized with RMSF at an annual rate of 48.2 per million population, compared with an estimated hospitalization rate of 16.9 per million Oklahoma residents. The majority of cases in the IHS database (69%) were diagnosed based on clinical suspicion rather than laboratory confirmation. The incidence of RMSF for Oklahoma American Indians as reported to the CDC was 37.4 cases per million, compared with 21.6 per million for all Oklahoma residents (RR 1.7, 95% confidence interval [CI] 1.5, 2.1). CONCLUSIONS: Rates derived from the IHS database may not be comparable to state and national rates because of differences in case inclusion criteria. However, an analysis of case report forms indicates that American Indians n Oklahoma have a significantly higher incidence of RMSF than that of the overall Oklahoma population. Oklahoma American Indians may benefit from educationa campaigns emphasizing prevention of tick bites and exposure to tick habitats.
PMCID: PMC1308603  PMID: 11236019
2.  Susceptibility of white-tailed deer (Odocoileus virginianus) to infection with Ehrlichia chaffeensis, the etiologic agent of human ehrlichiosis. 
Journal of Clinical Microbiology  1994;32(11):2725-2728.
Although more than 320 cases of human ehrlichiosis have been diagnosed in 27 states since 1986, the reservoir host or hosts remain unknown. Since antibodies reactive to Ehrlichia chaffeensis, the etiologic agent of human ehrlichiosis, have been found in white-tailed deer (Odocoileus virginianus), we experimentally evaluated the susceptibilities of four white-tailed deer to infection with E. chaffeensis and Ehrlichia canis, a closely related species. A fifth deer served as a negative control. Isolation and nested PCR amplification results from peripheral blood indicated that E. chaffeensis circulated for at least 2 weeks. The deer developed antibodies to E. chaffeensis by day 10 after inoculation, but there was no indication of clinical disease. Immunohistochemical staining identified E. chaffeensis within macrophage-type cells in lymph nodes. The deer inoculated with E. canis did not become infected and did not seroconvert. These results indicate that white-tailed deer can support an E. chaffeensis infection with resulting rickettsemia of at least 2 weeks. The resistance to infection and the absence of seroconversion upon exposure to E. canis indicate that antibody responses previously detected among wild deer are not E. canis cross-reactions. The role of deer as competent reservoirs in the life cycle of E. chaffeensis remains to be explored with suspected tick vectors.
PMCID: PMC264150  PMID: 7852563
3.  The epidemiology of bat rabies in New York State, 1988-92. 
Epidemiology and Infection  1994;113(3):501-511.
In 1993 New York and Texas each reported a human rabies case traced to a rare variant of rabies virus found in an uncommon species of bat. This study examined the epidemiology of bat rabies in New York State. Demographic, species, and animal-contact information for bats submitted for rabies testing from 1988-92 was analysed. The prevalence of rabies in 6810 bats was 4.6%. Nearly 90% of the 308 rabid bats identified to species were the common big brown bat (Eptesicus fuscus), which comprised 62% of all submissions. Only 25 submissions were silver-haired bats (Lasionycterus noctivagans), the species associated with the two 1993 human cases of rabies, and only two of these bats were positive. Rabies was most prevalent in female bats, in bats submitted because of human [corrected] contact, and in animals tested during September and October. These results highlight the unusual circumstances surrounding the recent human rabies cases in the United States. A species of bat rarely encountered by humans, and contributing little to the total rabies cases in bats, has been implicated in the majority of the indigenously acquired human rabies cases in the United States. The factors contributing to the transmission of this rare rabies variant remain unclear.
PMCID: PMC2271321  PMID: 7995360
4.  Association of intraspecific wounding with hantaviral infection in wild rats (Rattus norvegicus). 
Epidemiology and Infection  1988;101(2):459-472.
The potential for hantaviral transmission among wild Norway rats by wounding associated with aggressive interactions was evaluated using a prospective sero-epidemiological study coupled with a mark-release-recapture survey. There was a significant association between an animal's serological status and the presence of wounds. Longitudinal studies of marked and released animals showed seroconversion between captures was associated with wounding between captures more often (33%) than expected by chance, while unwounded animals seroconverted less often (8%) than expected. Typically, less than a 5% difference was found when comparing the incidence of seroconversion with the predicted rate based on wounding and seroprevalence. Infection was highly associated with the onset of sexual maturity and aggression but decoupled from rat age and the length of environmental exposure. Seroconversions occurred at times most associated with aggressive encounters and least associated with amicable behaviours that could lead to aerosol transmission.
PMCID: PMC2249393  PMID: 3141203
5.  Clinical and Serological Follow-Up of Patients with Human Granulocytic Ehrlichiosis in Slovenia 
An evaluation of the clinical outcome and the duration of the antibody response of patients with human granulocytic ehrlichiosis (HGE) was undertaken in Slovenia. Adult patients with a febrile illness occurring within 6 weeks of a tick bite were classified as having probable or confirmed HGE based on the outcome of serological or PCR testing. Thirty patients (median age, 44 years) were enrolled, and clinical evaluations and serum collection were undertaken at initial presentation and at 14 days, 6 to 8 weeks, and 3 to 4, 6, 12, 18, and 24 months. An indirect immunofluorescence assay (IFA) was performed, and reciprocal titers of ≥128 were interpreted as positive. Patients presented a median of 4 days after the onset of fever and were febrile for a median of 7.5 days; four (13.3%) received doxycycline. Seroconversion was observed in 3 of 30 (10.0%) patients, and 25 (83.3%) showed >4-fold change in antibody titer. PCR results were positive in 2 of 3 (66.7%) seronegative patients but in none of 27 seropositive patients at the first presentation. IFA antibody titers of ≥128 were found in 14 of 29 (48.3%), 17 of 30 (56.7%), 13 of 30 (43.4%), and 12 of 30 (40.0%) patients 6, 12, 18, and 24 months after presentation, respectively. Patients reporting additional tick bites during the study had significantly higher antibody titers at most time points during follow-up. No long-term clinical consequences were found during follow-up.
PMCID: PMC96168  PMID: 11527800
6.  Dual captures of Colorado rodents: implications for transmission of hantaviruses. 
Emerging Infectious Diseases  2000;6(4):363-369.
We analyzed dual-capture data collected during longitudinal studies monitoring transmission and persistence of Sin Nombre virus in rodents in Colorado. Our data indicate that multiple captures (two or more rodents captured in a single trap) may not be random, as indicated by previous studies, but rather the result of underlying, species-specific social behavior or cohesiveness. In the pairs we captured, most often, rodents were of the same species, were male, and could be recaptured as pairs. Therefore, dual captures of rodents, which are unusual but not rare, tend to occur among certain species, and appear to be nonrandom, group-foraging encounters. These demographic and ecologic characteristics may have implications for the study of the transmission of hantaviruses.
PMCID: PMC2640883  PMID: 10970147
7.  The human ehrlichioses in the United States. 
Emerging Infectious Diseases  1999;5(5):635-642.
The emerging tick-borne zoonoses human monocytic ehrlichiosis (HME) and human granulocytic ehrlichiosis (HGE) are under reported in the United States. From 1986 through 1997, 1,223 cases (742 HME, 449 HGE, and 32 not ascribed to a specific ehrlichial agent) were reported by state health departments. HME was most commonly reported from southeastern and southcentral states, while HGE was most often reported from northeastern and upper midwestern states. The annual number of reported cases increased sharply, from 69 in 1994 to 364 in 1997, coincident with an increase in the number of states making these conditions notifiable. From 1986 through 1997, 827 probable and confirmed cases were diagnosed by serologic testing at the Centers for Disease Control and Prevention, although how many of these cases were also reported by states is not known. Improved national surveillance would provide a better assessment of the public health importance of ehrlichiosis.
PMCID: PMC2627718  PMID: 10511519
8.  Long-term studies of hantavirus reservoir populations in the southwestern United States: a synthesis. 
Emerging Infectious Diseases  1999;5(1):135-142.
A series of intensive, longitudinal, mark-recapture studies of hantavirus infection dynamics in reservoir populations in the southwestern United States indicates consistent patterns as well as important differences among sites and host-virus associations. All studies found a higher prevalence of infection in older (particularly male) mice; one study associated wounds with seropositivity. These findings are consistent with horizontal transmission and transmission through fighting between adult male rodents. Despite very low rodent densities at some sites, low-level hantavirus infection continued, perhaps because of persistent infection in a few long-lived rodents or periodic reintroduction of virus from neighboring populations. Prevalence of hantavirus antibody showed seasonal and multiyear patterns that suggested a delayed density-dependent relationship between prevalence and population density. Clear differences in population dynamics and patterns of infection among sites, sampling periods, and host species underscore the importance of replication and continuity of long-term reservoir studies. Nevertheless, the measurable associations between environmental variables, reservoir population density, rates of virus transmission, and prevalence of infection in host populations may improve our capacity to model processes influencing infection and predict increased risk for hantavirus transmission to humans.
PMCID: PMC2627702  PMID: 10081681
9.  Long-term studies of hantavirus reservoir populations in the southwestern United States: rationale, potential, and methods. 
Emerging Infectious Diseases  1999;5(1):95-101.
Hantaviruses are rodent-borne zoonotic agents that cause hemorrhagic fever with renal syndrome in Asia and Europe and hantavirus pulmonary syndrome (HPS) in North and South America. The epidemiology of human diseases caused by these viruses is tied to the ecology of the rodent hosts, and effective control and prevention relies on a through understanding of host ecology. After the 1993 HPS outbreak in the southwestern United States, the Centers for Disease Control and Prevention initiated long-term studies of the temporal dynamics of hantavirus infection in host populations. These studies, which used mark-recapture techniques on 24 trapping webs at nine sites in the southwestern United States, were designed to monitor changes in reservoir population densities and in the prevalence and incidence of infection; quantify environmental factors associated with these changes; and when linked to surveillance databases for HPS, lead to predictive models of human risk to be used in the design and implementation of control and prevention measures for human hantavirus disease.
PMCID: PMC2627686  PMID: 10081676
10.  Identity of Ehrlichial DNA Sequences Derived from Ixodes ricinus Ticks with Those Obtained from Patients with Human Granulocytic Ehrlichiosis in Slovenia 
Journal of Clinical Microbiology  1999;37(1):209-210.
Adult Ixodes ricinus (Acari: Ixodidae) ticks collected near Ljubljana, Slovenia, were tested for the agent of human granulocytic ehrlichiosis (HGE) by using PCR assays based on the 16S rRNA gene. Three (3.2%) of 93 ticks were found to contain granulocytic ehrlichiae. Nucleotide sequences of portions of the bacterial groESL heat shock operon amplified from these ticks were identical or nearly (99.8%) identical to those previously determined for human patients with HGE from Slovenia, providing additional evidence that the ticks were infected with the HGE agent. This study identified I. ricinus as the likely vector for these ehrlichial pathogens of humans in this part of Europe.
PMCID: PMC84210  PMID: 9854093
11.  Ecologic studies of rodent reservoirs: their relevance for human health. 
Emerging Infectious Diseases  1998;4(4):529-537.
Within the past few years, the number of "new" human diseases associated with small-mammal reservoirs has increased dramatically, stimulating renewed interest in reservoir ecology research. A consistent, integrative approach to such research allows direct comparisons between studies, contributes to the efficient use of resources and data, and increases investigator safety. We outline steps directed toward understanding vertebrate host ecology as it relates to human disease and illustrate the relevance of each step by using examples from studies of hosts associated with rodent-borne hemorrhagic fever viruses.
PMCID: PMC2640244  PMID: 9866729
12.  Isolation and characterization of Ehrlichia chaffeensis strains from patients with fatal ehrlichiosis. 
Journal of Clinical Microbiology  1997;35(10):2496-2502.
Two new isolates of Ehrlichia chaffeensis (designated Jax and St. Vincent) were obtained from patients with fatal ehrlichial infections. Patients developed characteristic manifestations of severe disease due to E. chaffeensis, including marked thrombocytopenia, pulmonary insufficiency, and encephalopathy. Primary isolation was achieved in DH82 cells; the Jax and St. Vincent isolates were detected within 19 and 8 days postinoculation, respectively. The isolates were characterized by molecular evaluation of the 16S rRNA gene, the groESL heat shock operon, a 120-kDa immunodominant protein gene, and an incompletely characterized repetitive-motif sequence (variable-length PCR target [VLPT]). The sequences were compared with those of the corresponding molecular regions in the type isolate (Arkansas). St. Vincent contained one fewer repeat unit in both the 120-kDa protein gene and the VLPT compared with corresponding sequences of the Jax and Arkansas isolates. 16S rRNA gene sequences from the two new isolates had 100% identity to the corresponding sequences of the 91HE17 and Sapulpa isolates of E. chaffeensis, and to the corrected 16S rRNA gene sequence of the Arkansas isolate. The Jax isolate grew more slowly than the St. Vincent isolate in DH82 cells, and both of the new isolates grew more slowly than the extensively passaged Arkansas isolate. Although specific associations between ehrlichial pathogenicity and genotype were not identified from these comparisons, recovery of this organism from a spectrum of clinical presentations remains an integral step in understanding mechanisms of disease caused by E. chaffeensis.
PMCID: PMC229999  PMID: 9316896
13.  An indirect immunofluorescence assay using a cell culture-derived antigen for detection of antibodies to the agent of human granulocytic ehrlichiosis. 
Journal of Clinical Microbiology  1997;35(6):1510-1516.
An indirect immunofluorescence assay for the detection of human antibodies to the agent of human granulocytic ehrlichiosis (HGE) was developed and standardized. Antigen was prepared from a human promyelocytic leukemia cell line (HL-60) infected with a tick-derived isolate of the HGE agent (USG3). Suitable antigen presentation and preservation of cellular morphology were obtained when infected cells were applied and cultured on the slide, excess medium was removed, and cells were fixed with acetone. Use of a buffer containing bovine serum albumin and goat serum reduced background fluorescence, and use of an immunoglobulin G (gamma-specific) conjugate reduced nonspecific binding. The assay readily detected specific antibody from HGE patients and did not detect antibody from healthy individuals. No significant reactivity was noted in sera from patients with high titers of antibodies to other rickettsial species. We were able to identify antibodies reactive to USG3 antigen in samples from areas where HGE is endemic that had tested negative to other rickettsial agents. Animal sera reactive against Ehrlichia equi or Ehrlichia phagocytophila bound to the HGE antigen, indicating that the assay may be useful for veterinary use. Comparability between two different laboratories was assessed by using coded human sera exchanged between laboratories. Results from the two laboratories were similar, indicating that the assay can be easily integrated into use for routine testing for HGE. The assay was then compared to an assay using horse neutrophils infected with ehrlichiae. The two assays gave comparable results, indicating that the cell culture-derived antigen can be used for testing samples that have been previously tested with E. equi as an antigen. The new assay offers several advantages over other immunofluorescence methods that use animal-derived antigen and is suitable for use in testing for human antibodies to the HGE agent.
PMCID: PMC229776  PMID: 9163471
14.  The ascension of wildlife rabies: a cause for public health concern or intervention? 
Emerging Infectious Diseases  1995;1(4):107-114.
The epidemiology of rabies in the United States has changed substantially during the last half century, as the source of the disease has changed from domesticated animals to wildlife, principally raccoons, skunks, foxes, and bats. Moreover, the changes observed among affected wildlife populations have not occurred without human influence. Rather, human attraction to the recreational and economic resources provided by wildlife has contributed to the reemergence of rabies as a major zoonosis. Although human deaths caused by rabies have declined recently to an average of one or two per year, the estimated costs associated with the decrease in deaths amount to hundreds of millions of dollars annually. In future efforts to control rabies harbored by free-ranging animal reservoirs, public health professionals will have to apply imaginative, safe, and cost-effective solutions to this age-old malady in addition to using traditional measures.
PMCID: PMC2626887  PMID: 8903179
15.  Current issues in rabies prevention in the United States health dilemmas. Public coffers, private interests. 
Public Health Reports  1996;111(5):400-407.
OVER THE LAST 100 years, rabies in the United States has changed dramatically. More than 90% of all animal rabies cases reported annually to the CDC now occur in wildlife, whereas before 1960 the majority were in domestic animals. The principal rabies hosts today are wild carnivores and bats infected with several viral variants. Annual human deaths have fallen from more than a hundred at the turn of the century to one to two per year despite major outbreaks of animal rabies in several geographic areas. Modern day prophylaxis has proven nearly 100% successful; most human fatalities now occur in people who fail to seek medical treatment, usually because they do not recognize a risk in the animal contact leading to the infection. Although these human rabies deaths are rare, the estimated public health costs associated with disease detection, prevention, and control have risen, exceeding millions of dollars each year. Cost considerations must be weighed along with other factors in addressing issues such as the appropriate handling of nontraditional and exotic pets, future guidelines for rabies prophylaxis, and novel methods of disease prevention.
PMCID: PMC1381782  PMID: 8837628
16.  Comparison of polymerase chain reaction and culture for detection of Borrelia burgdorferi in naturally infected Peromyscus leucopus and experimentally infected C.B-17 scid/scid mice. 
Journal of Clinical Microbiology  1992;30(10):2625-2631.
Culture and the polymerase chain reaction (PCR) were compared for detection of Borrelia burgdorferi infection in wild-caught Peromyscus leucopus and experimentally inoculated C.B-17 scid/scid (severe combined immunodeficient) mice. PCR targeted highly conserved regions of the ospA gene and could detect one to five cultured organisms and 10 to 50 copies of molecularly cloned ospA DNA. Organs (kidney, spleen, and urinary bladder) and/or ear biopsy samples were obtained from 108 captured P. leucopus mice, and tissues were obtained from 7 experimentally inoculated mice. A simple sample-processing procedure with proteinase K and detergent treatment was used in the PCR analysis. Overall, B. burgdorferi was detected in 29 of 108 (27%) P. leucopus mice by culture and in 31 of 108 (29%) mice by PCR. As assessed by the kappa statistic, agreement between PCR and culture was high for ear and bladder (kappa = 0.80 and 0.65, respectively) and low for kidney and spleen (kappa = 0.37 and 0.03, respectively). While concordant results were obtained from 98 animals, PCR detected B. burgdorferi from 6 additional mice for which cultures were negative and culture detected B. burgdorferi from 4 animals which were PCR negative. Further phenol-chloroform extraction of DNA in a limited number of samples improved the sensitivity of PCR compared with that of culture. These results indicate that PCR may be as sensitive as culture for detecting B. burgdorferi in ear samples and that PCR analysis is suitable for establishing the infection status of animals in mark-release-recapture studies.
PMCID: PMC270489  PMID: 1400962

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