Co-Infection of Blacklegged Ticks with Babesia microti and Borrelia burgdorferi Is Higher than Expected and Acquired from Small Mammal Hosts
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{"title"=>"Co-infection of blacklegged ticks with Babesia microti and Borrelia burgdorferi is higher than expected and acquired from small mammal hosts", "type"=>"journal", "authors"=>[{"first_name"=>"Michelle H.", "last_name"=>"Hersh", "scopus_author_id"=>"14063256900"}, {"first_name"=>"Richard S.", "last_name"=>"Ostfeld", "scopus_author_id"=>"7006957295"}, {"first_name"=>"Diana J.", "last_name"=>"McHenry", "scopus_author_id"=>"16241959000"}, {"first_name"=>"Michael", "last_name"=>"Tibbetts", "scopus_author_id"=>"23483331000"}, {"first_name"=>"Jesse L.", "last_name"=>"Brunner", "scopus_author_id"=>"7102413648"}, {"first_name"=>"Mary E.", "last_name"=>"Killilea", "scopus_author_id"=>"24335016800"}, {"first_name"=>"Kathleen", "last_name"=>"LoGiudice", "scopus_author_id"=>"6602497313"}, {"first_name"=>"Kenneth A.", "last_name"=>"Schmidt", "scopus_author_id"=>"55464606000"}, {"first_name"=>"Felicia", "last_name"=>"Keesing", "scopus_author_id"=>"6701906870"}], "year"=>2014, "source"=>"PLoS ONE", "identifiers"=>{"scopus"=>"2-s2.0-84903287452", "doi"=>"10.1371/journal.pone.0099348", "sgr"=>"84903287452", "pmid"=>"24940999", "issn"=>"19326203", "pui"=>"373396754"}, "id"=>"bd8e3fc1-b621-3d90-84d6-55c7432f5593", "abstract"=>"Humans in the northeastern and midwestern United States are at increasing risk of acquiring tickborne diseases – not only Lyme disease, but also two emerging diseases, human granulocytic anaplasmosis and human babesiosis. Co-infection with two or more of these pathogens can increase the severity of health impacts. The risk of co-infection is intensified by the ecology of these three diseases because all three pathogens (Borrelia burgdorferi, Anaplasma phagocytophilum, and Babesia microti) are transmitted by the same vector, blacklegged ticks (Ixodes scapularis), and are carried by many of the same reservoir hosts. The risk of exposure to multiple pathogens from a single tick bite and the sources of co-infected ticks are not well understood. In this study, we quantify the risk of co-infection by measuring infection prevalence in 4,368 questing nymphs throughout an endemic region for all three diseases (Dutchess County, NY) to determine if co-infections occur at frequencies other than predicted by independent assortment of pathogens. Further, we identify sources of co-infection by quantifying rates of co-infection on 3,275 larval ticks fed on known hosts. We find significant deviations of levels of co-infection in questing nymphs, most notably 83% more co-infection with Babesia microti and Borrelia burgdorferi than predicted by chance alone. Further, this pattern of increased co-infection was observed in larval ticks that fed on small mammal hosts, but not on meso-mammal, sciurid, or avian hosts. Co-infections involving A. phagocytophilum were less common, and fewer co-infections of A. phagocytophilum and B. microti than predicted by chance were observed in both questing nymphs and larvae fed on small mammals. Medical practitioners should be aware of the elevated risk of B. microti/B. burgdorferi co-infection.", "link"=>"http://www.mendeley.com/research/coinfection-blacklegged-ticks-babesia-microti-borrelia-burgdorferi-higher-expected-acquired-small-ma", "reader_count"=>65, "reader_count_by_academic_status"=>{"Unspecified"=>1, "Professor > Associate Professor"=>4, "Librarian"=>1, "Student > Doctoral Student"=>3, "Researcher"=>15, "Student > Ph. D. Student"=>12, "Student > Postgraduate"=>5, "Other"=>5, "Student > Master"=>7, "Student > Bachelor"=>8, "Lecturer > Senior Lecturer"=>1, "Professor"=>3}, "reader_count_by_user_role"=>{"Unspecified"=>1, "Professor > Associate Professor"=>4, "Librarian"=>1, "Student > Doctoral Student"=>3, "Researcher"=>15, "Student > Ph. D. Student"=>12, "Student > Postgraduate"=>5, "Other"=>5, "Student > Master"=>7, "Student > Bachelor"=>8, "Lecturer > Senior Lecturer"=>1, "Professor"=>3}, "reader_count_by_subject_area"=>{"Unspecified"=>2, "Agricultural and Biological Sciences"=>32, "Arts and Humanities"=>1, "Philosophy"=>1, "Veterinary Science and Veterinary Medicine"=>5, "Business, Management and Accounting"=>1, "Earth and Planetary Sciences"=>1, "Environmental Science"=>4, "Biochemistry, Genetics and Molecular Biology"=>4, "Nursing and Health Professions"=>1, "Medicine and Dentistry"=>6, "Design"=>1, "Psychology"=>1, "Social Sciences"=>1, "Immunology and Microbiology"=>4}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>6}, "Social Sciences"=>{"Social Sciences"=>1}, "Psychology"=>{"Psychology"=>1}, "Unspecified"=>{"Unspecified"=>2}, "Environmental Science"=>{"Environmental Science"=>4}, "Arts and Humanities"=>{"Arts and Humanities"=>1}, "Design"=>{"Design"=>1}, "Earth and Planetary Sciences"=>{"Earth and Planetary Sciences"=>1}, "Immunology and Microbiology"=>{"Immunology and Microbiology"=>4}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>32}, "Business, Management and Accounting"=>{"Business, Management and Accounting"=>1}, "Nursing and Health Professions"=>{"Nursing and Health Professions"=>1}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>4}, "Philosophy"=>{"Philosophy"=>1}, "Veterinary Science and Veterinary Medicine"=>{"Veterinary Science and Veterinary Medicine"=>5}}, "reader_count_by_country"=>{"United States"=>1, "Japan"=>1, "United Kingdom"=>1}, "group_count"=>3}

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  • {"files"=>["https://ndownloader.figshare.com/files/1538977"], "description"=>"<p>Bolded <i>p-</i>values are significant at α = 0.05.</p>", "links"=>[], "tags"=>["ecology", "Community Ecology", "Ecological risk", "organisms", "animals", "invertebrates", "arthropoda", "arachnida", "ixodes", "ticks", "Veterinary science", "Veterinary diseases", "Zoonoses", "epidemiology", "disease vectors", "Vector biology", "Infectious diseases", "Bacterial diseases", "Borrelia infection", "Lyme disease", "Human granulocytic anaplasmosis", "Emerging infectious diseases", "Parasitic diseases", "babesiosis", "Public and occupational health", "disease ecology", "prevalence", "host-collected", "fed", "meso-mammals", "permutation", "assuming", "assortment", "deviations", "observed"], "article_id"=>1060940, "categories"=>["Biological Sciences"], "users"=>["Michelle H. Hersh", "Richard S. Ostfeld", "Diana J. McHenry", "Michael Tibbetts", "Jesse L. Brunner", "Mary E. Killilea", "Kathleen LoGiudice", "Kenneth A. Schmidt", "Felicia Keesing"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0099348.t003", "stats"=>{"downloads"=>1, "page_views"=>8, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Predictions_of_infection_prevalence_in_host_collected_ticks_fed_on_meso_mammals_using_a_permutation_analysis_assuming_independent_assortment_of_all_three_pathogens_and_deviations_of_observed_data_from_those_predictions_/1060940", "title"=>"Predictions of infection prevalence in host-collected ticks fed on meso-mammals using a permutation analysis assuming independent assortment of all three pathogens, and deviations of observed data from those predictions.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2014-06-18 03:30:47"}
  • {"files"=>["https://ndownloader.figshare.com/files/1538974"], "description"=>"<p>Mean co-infection prevalence for Anaplasma phagocytophilum (Ap), Babesia microti (Bm), and Borrelia burgdorferi (Bb) of host-collected Ixodes scapularis ticks fed on (A) small mammal, (B) meso-mammal, (C) sciurid, and (D) bird host species. Each category represents the mean prevalence of each specific co-infection type as opposed to overall prevalence. Error bars show standard error. Note that no co-infections were observed in D. carolinensis.</p>", "links"=>[], "tags"=>["ecology", "Community Ecology", "Ecological risk", "organisms", "animals", "invertebrates", "arthropoda", "arachnida", "ixodes", "ticks", "Veterinary science", "Veterinary diseases", "Zoonoses", "epidemiology", "disease vectors", "Vector biology", "Infectious diseases", "Bacterial diseases", "Borrelia infection", "Lyme disease", "Human granulocytic anaplasmosis", "Emerging infectious diseases", "Parasitic diseases", "babesiosis", "Public and occupational health", "disease ecology", "prevalence", "anaplasma", "Babesia", "borrelia", "burgdorferi"], "article_id"=>1060937, "categories"=>["Biological Sciences"], "users"=>["Michelle H. Hersh", "Richard S. Ostfeld", "Diana J. McHenry", "Michael Tibbetts", "Jesse L. Brunner", "Mary E. Killilea", "Kathleen LoGiudice", "Kenneth A. Schmidt", "Felicia Keesing"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0099348.g003", "stats"=>{"downloads"=>4, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Co_infection_prevalence_of_Anaplasma_phagocytophilum_Babesia_microti_and_Borrelia_burgdorferi_in_wildlife_host_species_groups_/1060937", "title"=>"Co-infection prevalence of Anaplasma phagocytophilum, Babesia microti, and Borrelia burgdorferi in wildlife host species groups.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-06-18 03:30:47"}
  • {"files"=>["https://ndownloader.figshare.com/files/1538972"], "description"=>"<p>Mean levels of co-infection with <i>Anaplasma phagocytophilum</i> (Ap), <i>Babesia microti</i> (Bm), and <i>Borrelia burgdorferi</i> (Bb) in questing nymphal <i>Ixodes scapularis</i> ticks by site, 2011–2012. Each category represents mean overall prevalence as opposed to the prevalence of each specific infection type – for example, the “Ap” bar represents not just single infections but also ticks co-infected with Ap and either or both of the other two pathogens. Error bars represent standard error. For individual years see <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0099348#pone.0099348.s002\" target=\"_blank\">Figure S2</a>.</p>", "links"=>[], "tags"=>["ecology", "Community Ecology", "Ecological risk", "organisms", "animals", "invertebrates", "arthropoda", "arachnida", "ixodes", "ticks", "Veterinary science", "Veterinary diseases", "Zoonoses", "epidemiology", "disease vectors", "Vector biology", "Infectious diseases", "Bacterial diseases", "Borrelia infection", "Lyme disease", "Human granulocytic anaplasmosis", "Emerging infectious diseases", "Parasitic diseases", "babesiosis", "Public and occupational health", "disease ecology", "co-infection", "prevalence", "Babesia", "questing"], "article_id"=>1060935, "categories"=>["Biological Sciences"], "users"=>["Michelle H. Hersh", "Richard S. Ostfeld", "Diana J. McHenry", "Michael Tibbetts", "Jesse L. Brunner", "Mary E. Killilea", "Kathleen LoGiudice", "Kenneth A. Schmidt", "Felicia Keesing"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0099348.g001", "stats"=>{"downloads"=>0, "page_views"=>11, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Mean_levels_of_co_infection_prevalence_of_Anaplasma_phagocytophilum_Babesia_microti_and_Borrelia_burgdorferi_in_questing_Ixodes_scapularis_nymphs_by_site_/1060935", "title"=>"Mean levels of co-infection prevalence of <i>Anaplasma phagocytophilum, Babesia microti</i>, and <i>Borrelia burgdorferi</i> in questing <i>Ixodes scapularis</i> nymphs, by site.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-06-18 03:30:47"}
  • {"files"=>["https://ndownloader.figshare.com/files/1538973"], "description"=>"<p>Log (base 2) of observed: expected ratio of each infection status of questing <i>Ixodes scapularis</i> ticks sampled at 161 sites across Dutchess County, NY, USA. The magnitude and direction of the log ratios illustrates the extent to which the observed levels of co-infection differed from expected levels of co-infection due to random assortment of pathogens. Pathogens sampled include <i>Anaplasma phagocytophilum</i> (Ap), <i>Babesia microti</i> (Bm), and <i>Borrelia burgdorferi</i> (Bb). Expected infection frequencies are based on 100,000 random permutations of infection frequencies for each pathogen.</p>", "links"=>[], "tags"=>["ecology", "Community Ecology", "Ecological risk", "organisms", "animals", "invertebrates", "arthropoda", "arachnida", "ixodes", "ticks", "Veterinary science", "Veterinary diseases", "Zoonoses", "epidemiology", "disease vectors", "Vector biology", "Infectious diseases", "Bacterial diseases", "Borrelia infection", "Lyme disease", "Human granulocytic anaplasmosis", "Emerging infectious diseases", "Parasitic diseases", "babesiosis", "Public and occupational health", "disease ecology", "questing"], "article_id"=>1060936, "categories"=>["Biological Sciences"], "users"=>["Michelle H. Hersh", "Richard S. Ostfeld", "Diana J. McHenry", "Michael Tibbetts", "Jesse L. Brunner", "Mary E. Killilea", "Kathleen LoGiudice", "Kenneth A. Schmidt", "Felicia Keesing"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0099348.g002", "stats"=>{"downloads"=>2, "page_views"=>6, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Log_base_2_of_the_observed_expected_ratio_of_questing_Ixodes_scapularis_nymphs_/1060936", "title"=>"Log (base 2) of the observed: expected ratio of questing <i>Ixodes scapularis</i> nymphs.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-06-18 03:30:47"}
  • {"files"=>["https://ndownloader.figshare.com/files/1538980", "https://ndownloader.figshare.com/files/1538981", "https://ndownloader.figshare.com/files/1538982", "https://ndownloader.figshare.com/files/1538983", "https://ndownloader.figshare.com/files/1538984", "https://ndownloader.figshare.com/files/1538985"], "description"=>"<div><p>Humans in the northeastern and midwestern United States are at increasing risk of acquiring tickborne diseases – not only Lyme disease, but also two emerging diseases, human granulocytic anaplasmosis and human babesiosis. Co-infection with two or more of these pathogens can increase the severity of health impacts. The risk of co-infection is intensified by the ecology of these three diseases because all three pathogens (<i>Borrelia burgdorferi, Anaplasma phagocytophilum</i>, and <i>Babesia microti</i>) are transmitted by the same vector, blacklegged ticks (<i>Ixodes scapularis</i>), and are carried by many of the same reservoir hosts. The risk of exposure to multiple pathogens from a single tick bite and the sources of co-infected ticks are not well understood. In this study, we quantify the risk of co-infection by measuring infection prevalence in 4,368 questing nymphs throughout an endemic region for all three diseases (Dutchess County, NY) to determine if co-infections occur at frequencies other than predicted by independent assortment of pathogens. Further, we identify sources of co-infection by quantifying rates of co-infection on 3,275 larval ticks fed on known hosts. We find significant deviations of levels of co-infection in questing nymphs, most notably 83% more co-infection with <i>Babesia microti</i> and <i>Borrelia burgdorferi</i> than predicted by chance alone. Further, this pattern of increased co-infection was observed in larval ticks that fed on small mammal hosts, but not on meso-mammal, sciurid, or avian hosts. Co-infections involving <i>A. phagocytophilum</i> were less common, and fewer co-infections of <i>A. phagocytophilum</i> and <i>B. microti</i> than predicted by chance were observed in both questing nymphs and larvae fed on small mammals. Medical practitioners should be aware of the elevated risk of <i>B. microti</i>/<i>B. burgdorferi</i> co-infection.</p></div>", "links"=>[], "tags"=>["ecology", "Community Ecology", "Ecological risk", "organisms", "animals", "invertebrates", "arthropoda", "arachnida", "ixodes", "ticks", "Veterinary science", "Veterinary diseases", "Zoonoses", "epidemiology", "disease vectors", "Vector biology", "Infectious diseases", "Bacterial diseases", "Borrelia infection", "Lyme disease", "Human granulocytic anaplasmosis", "Emerging infectious diseases", "Parasitic diseases", "babesiosis", "Public and occupational health", "disease ecology", "co-infection", "blacklegged", "higher", "acquired", "mammal", "hosts"], "article_id"=>1060943, "categories"=>["Biological Sciences"], "users"=>["Michelle H. Hersh", "Richard S. Ostfeld", "Diana J. McHenry", "Michael Tibbetts", "Jesse L. Brunner", "Mary E. Killilea", "Kathleen LoGiudice", "Kenneth A. Schmidt", "Felicia Keesing"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0099348.s001", "https://dx.doi.org/10.1371/journal.pone.0099348.s002", "https://dx.doi.org/10.1371/journal.pone.0099348.s003", "https://dx.doi.org/10.1371/journal.pone.0099348.s004", "https://dx.doi.org/10.1371/journal.pone.0099348.s005", "https://dx.doi.org/10.1371/journal.pone.0099348.s006"], "stats"=>{"downloads"=>1, "page_views"=>6, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Co_Infection_of_Blacklegged_Ticks_with_Babesia_microti_and_Borrelia_burgdorferi_Is_Higher_than_Expected_and_Acquired_from_Small_Mammal_Hosts/1060943", "title"=>"Co-Infection of Blacklegged Ticks with <i>Babesia microti</i> and <i>Borrelia burgdorferi</i> Is Higher than Expected and Acquired from Small Mammal Hosts", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2014-06-18 03:30:47"}
  • {"files"=>["https://ndownloader.figshare.com/files/1538979"], "description"=>"<p>Bolded <i>p-</i>values are significant at α = 0.05.</p>", "links"=>[], "tags"=>["ecology", "Community Ecology", "Ecological risk", "organisms", "animals", "invertebrates", "arthropoda", "arachnida", "ixodes", "ticks", "Veterinary science", "Veterinary diseases", "Zoonoses", "epidemiology", "disease vectors", "Vector biology", "Infectious diseases", "Bacterial diseases", "Borrelia infection", "Lyme disease", "Human granulocytic anaplasmosis", "Emerging infectious diseases", "Parasitic diseases", "babesiosis", "Public and occupational health", "disease ecology", "prevalence", "questing", "nymphal", "permutation", "assuming", "assortment", "deviations", "observed"], "article_id"=>1060942, "categories"=>["Biological Sciences"], "users"=>["Michelle H. Hersh", "Richard S. Ostfeld", "Diana J. McHenry", "Michael Tibbetts", "Jesse L. Brunner", "Mary E. Killilea", "Kathleen LoGiudice", "Kenneth A. Schmidt", "Felicia Keesing"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0099348.t001", "stats"=>{"downloads"=>0, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Predictions_of_infection_prevalence_in_questing_Ixodes_scapularis_nymphal_ticks_using_a_permutation_analysis_assuming_independent_assortment_of_all_three_pathogens_and_deviations_of_observed_data_from_those_predictions_/1060942", "title"=>"Predictions of infection prevalence in questing <i>Ixodes scapularis</i> nymphal ticks using a permutation analysis assuming independent assortment of all three pathogens, and deviations of observed data from those predictions.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2014-06-18 03:30:47"}
  • {"files"=>["https://ndownloader.figshare.com/files/1538976"], "description"=>"<p>Bolded <i>p-</i>values are significant at α = 0.05.</p>", "links"=>[], "tags"=>["ecology", "Community Ecology", "Ecological risk", "organisms", "animals", "invertebrates", "arthropoda", "arachnida", "ixodes", "ticks", "Veterinary science", "Veterinary diseases", "Zoonoses", "epidemiology", "disease vectors", "Vector biology", "Infectious diseases", "Bacterial diseases", "Borrelia infection", "Lyme disease", "Human granulocytic anaplasmosis", "Emerging infectious diseases", "Parasitic diseases", "babesiosis", "Public and occupational health", "disease ecology", "prevalence", "host-collected", "fed", "sciurids", "permutation", "assuming", "assortment", "deviations", "observed"], "article_id"=>1060939, "categories"=>["Biological Sciences"], "users"=>["Michelle H. Hersh", "Richard S. Ostfeld", "Diana J. McHenry", "Michael Tibbetts", "Jesse L. Brunner", "Mary E. Killilea", "Kathleen LoGiudice", "Kenneth A. Schmidt", "Felicia Keesing"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0099348.t004", "stats"=>{"downloads"=>1, "page_views"=>9, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Predictions_of_infection_prevalence_in_host_collected_ticks_fed_on_sciurids_using_a_permutation_analysis_assuming_independent_assortment_of_all_three_pathogens_and_deviations_of_observed_data_from_those_predictions_/1060939", "title"=>"Predictions of infection prevalence in host-collected ticks fed on sciurids using a permutation analysis assuming independent assortment of all three pathogens, and deviations of observed data from those predictions.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2014-06-18 03:30:47"}
  • {"files"=>["https://ndownloader.figshare.com/files/1538975"], "description"=>"<p>Bolded <i>p-</i>values are significant at α = 0.05.</p>", "links"=>[], "tags"=>["ecology", "Community Ecology", "Ecological risk", "organisms", "animals", "invertebrates", "arthropoda", "arachnida", "ixodes", "ticks", "Veterinary science", "Veterinary diseases", "Zoonoses", "epidemiology", "disease vectors", "Vector biology", "Infectious diseases", "Bacterial diseases", "Borrelia infection", "Lyme disease", "Human granulocytic anaplasmosis", "Emerging infectious diseases", "Parasitic diseases", "babesiosis", "Public and occupational health", "disease ecology", "prevalence", "host-collected", "fed", "birds", "permutation", "assuming", "assortment", "deviations", "observed"], "article_id"=>1060938, "categories"=>["Biological Sciences"], "users"=>["Michelle H. Hersh", "Richard S. Ostfeld", "Diana J. McHenry", "Michael Tibbetts", "Jesse L. Brunner", "Mary E. Killilea", "Kathleen LoGiudice", "Kenneth A. Schmidt", "Felicia Keesing"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0099348.t005", "stats"=>{"downloads"=>0, "page_views"=>2, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Predictions_of_infection_prevalence_in_host_collected_ticks_fed_on_birds_using_a_permutation_analysis_assuming_independent_assortment_of_all_three_pathogens_and_deviations_of_observed_data_from_those_predictions_/1060938", "title"=>"Predictions of infection prevalence in host-collected ticks fed on birds using a permutation analysis assuming independent assortment of all three pathogens, and deviations of observed data from those predictions.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2014-06-18 03:30:47"}

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