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      Rickettsial Infections among Ctenocephalides felis and Host Animals during a Flea-Borne Rickettsioses Outbreak in Orange County, California

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          Abstract

          Due to a resurgence of flea-borne rickettsioses in Orange County, California, we investigated the etiologies of rickettsial infections of Ctenocephalides felis, the predominant fleas species obtained from opossums ( Didelphis virginiana) and domestic cats ( Felis catus), collected from case exposure sites and other areas in Orange County. In addition, we assessed the prevalence of IgG antibodies against spotted fever group (SFGR) and typhus group (TGR) rickettsiae in opossum sera. Of the 597 flea specimens collected from opossums and cats, 37.2% tested positive for Rickettsia. PCR and sequencing of rickettsial genes obtained from C. felis flea DNA preparations revealed the presence of R. typhi (1.3%), R. felis (28.0%) and R. felis-like organisms (7.5%). Sera from opossums contained TGR-specific (40.84%), but not SFGR-specific antibodies. The detection of R. felis and R. typhi in the C. felis fleas in Orange County highlights the potential risk for human infection with either of these pathogens, and underscores the need for further investigations incorporating specimens from humans, animal hosts, and invertebrate vectors in endemic areas. Such studies will be essential for establishing a link in the ongoing flea-borne rickettsioses outbreaks.

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          Most cited references37

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          Murine typhus: an unrecognized suburban vectorborne disease.

          Murine typhus, an acute febrile illness caused by Rickettsia typhi, is distributed worldwide. Mainly transmitted by the fleas of rodents, it is associated with cities and ports where urban rats (Rattus rattus and Rattus norvegicus) are abundant. In the United States, cases are concentrated in suburban areas of Texas and California. Contrary to the classic rat-flea-rat cycle, the most important reservoirs of infection in these areas are opossums and cats. The cat flea, Ctenocephalides felis, has been identified as the principal vector. In Texas, murine typhus cases occur in spring and summer, whereas, in California, cases have been documented in summer and fall. Most patients present with fever, and many have rash and headache. Serologic testing with the indirect immunofluorescence assay is the preferred diagnostic method. Doxycycline is the antibiotic of choice and has been shown to shorten the course of illness.
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            Flea-borne rickettsioses: ecologic considerations.

            Ecologic and economic factors, as well as changes in human behavior, have resulted in the emergence of new and the reemergence of existing but forgotten infectious diseases during the past 20 years. Flea-borne disease organisms (e.g., Yersinia pestis, Rickettsia typhi, R. felis, and Bartonella henselae) are widely distributed throughout the world in endemic-disease foci, where components of the enzootic cycle are present. However, flea-borne diseases could reemerge in epidemic form because of changes in vector-host ecology due to environmental and human behavior modification. The changing ecology of murine typhus in southern California and Texas over the past 30 years is a good example of urban and suburban expansion affecting infectious disease outbreaks. In these areas, the classic rat-flea-rat cycle of R. typhi has been replaced by a peridomestic animal cycle involving, e.g., free-ranging cats, dogs, and opossums and their fleas. In addition to the vector-host components of the murine typhus cycle, we have uncovered a second typhuslike rickettsia, R. felis. This agent was identified from the blood of a hospitalized febrile patient and from opossums and their fleas. We reviewed the ecology of R. typhi and R. felis and present recent data relevant to the vector biology, immunology, and molecular characterization and phylogeny of flea-borne rickettsioses.
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              Rickettsia felis: from a rare disease in the USA to a common cause of fever in sub-Saharan Africa.

              P. Parola (2011)
              Rickettsia felis is a spotted fever group rickettsia that has been definitely described in 2002. Within the last 20 years, there have been a growing number of reports implicating R. felis as a human pathogen, parallel to the fast-growing reports of the worldwide detection of R. felis in arthropod hosts, mainly the cat flea Ctenocephalides felis felis. R. felis is now known as the agent of the so-called flea-borne spotted fever, with more than 70 cases documented in the literature. Recently, two studies respectively conducted in Senegal and Kenya, have challenged the importance of R. felis infection in patients with unexplained fever in sub-Saharan Africa. We focus here on the epidemiological and clinical aspects of R. felis infection. More studies are needed, including the study of other arthropod vectors, but it can be speculated that R. felis infection might be an important neglected agent of fever in sub-Saharan Africa. © 2011 The Author. Clinical Microbiology and Infection © 2011 European Society of Clinical Microbiology and Infectious Diseases.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                18 August 2016
                2016
                : 11
                : 8
                : e0160604
                Affiliations
                [1 ]Naval Medical Research Center, Silver Spring, MD, United States of America
                [2 ]Orange County Mosquito and Vector Control District, Garden Grove, CA, United States of America
                [3 ]Louisiana State University, Baton Rouge, LA, United States of America
                [4 ]Shippensburg University, Shippensburg, PA, United States of America
                [5 ]West Valley Mosquito and Vector Control District, Ontario, CA, United States of America
                Director of Laboratory Sciences, UNITED STATES
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                • Conceptualization: RFC LK CF SB.

                • Data curation: ANM LK ALF.

                • Formal analysis: LK ANM SB KN.

                • Funding acquisition: ALR.

                • Investigation: SS SB KRM.

                • Methodology: CF AO ANM CMF.

                • Project administration: RFC LK ALR.

                • Resources: ALR KRM RFC.

                • Supervision: JJ RFC.

                • Validation: AO ANM CMF.

                • Visualization: KN CMF.

                • Writing - original draft: ANM.

                • Writing - review & editing: CMF ALF LK RFC ALR.

                Author information
                http://orcid.org/0000-0002-0248-8463
                Article
                PONE-D-16-16369
                10.1371/journal.pone.0160604
                4990410
                27537367
                60d5c4d1-9d44-4016-b7a4-022d5a288c92

                This is an open access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication.

                History
                : 22 April 2016
                : 21 July 2016
                Page count
                Figures: 2, Tables: 2, Pages: 13
                Funding
                Funded by: Global Emerging Infections Surveillance and Response System
                Award ID: 847705.82000.25G.A0074
                Award Recipient :
                This work was supported by the Global Emerging Infections Surveillance and Response System, a Division of the Armed Forces Health Surveillance Center, work unit number 847705.82000.25GB.A0074 ( https://www.afhsc.mil/Home/Sections/GEIS). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology and Life Sciences
                Organisms
                Animals
                Invertebrates
                Arthropoda
                Insects
                Fleas
                Biology and Life Sciences
                Organisms
                Animals
                Vertebrates
                Amniotes
                Mammals
                Marsupials
                Opossums
                Biology and Life Sciences
                Organisms
                Animals
                Vertebrates
                Amniotes
                Mammals
                Cats
                Biology and Life Sciences
                Organisms
                Bacteria
                Rickettsia
                Biology and Life Sciences
                Microbiology
                Medical Microbiology
                Microbial Pathogens
                Bacterial Pathogens
                Rickettsia
                Medicine and Health Sciences
                Pathology and Laboratory Medicine
                Pathogens
                Microbial Pathogens
                Bacterial Pathogens
                Rickettsia
                Research and Analysis Methods
                Immunologic Techniques
                Immunoassays
                Enzyme-Linked Immunoassays
                People and places
                Geographical locations
                North America
                United States
                California
                Biology and Life Sciences
                Molecular Biology
                Molecular Biology Techniques
                Artificial Gene Amplification and Extension
                Polymerase Chain Reaction
                Research and Analysis Methods
                Molecular Biology Techniques
                Artificial Gene Amplification and Extension
                Polymerase Chain Reaction
                Biology and Life Sciences
                Physiology
                Immune Physiology
                Antibodies
                Medicine and Health Sciences
                Physiology
                Immune Physiology
                Antibodies
                Biology and Life Sciences
                Immunology
                Immune System Proteins
                Antibodies
                Medicine and Health Sciences
                Immunology
                Immune System Proteins
                Antibodies
                Biology and Life Sciences
                Biochemistry
                Proteins
                Immune System Proteins
                Antibodies
                Custom metadata
                All relevant data are within the paper and its supporting files. Additional data is also available from the GenBanks accession numbers KT304218, KT304219, KT304220.

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