Strains of Anaplasma phagocytophilum from horses in Ohio are related to isolates from humans in the northeastern USA

ABSTRACT The tick-borne obligatory intracellular bacterium Anaplasma phagocytophilum infects granulocytes of humans as well as domesticated and wild animals, causing a febrile disease collectively called granulocytic anaplasmosis. The host species specificity and zoonotic potential of A. phagocytoph...

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Main Authors: Rory C. Chien, Lin Mingqun, Qi Yan, Nina Randolph, Weiyan Huang, Maxey Wellman, Ramiro Toribio, Yasuko Rikihisa
Format: Article
Language:English
Published: American Society for Microbiology 2023-12-01
Series:Microbiology Spectrum
Subjects:
Online Access:https://journals.asm.org/doi/10.1128/spectrum.02632-23
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author Rory C. Chien
Lin Mingqun
Qi Yan
Nina Randolph
Weiyan Huang
Maxey Wellman
Ramiro Toribio
Yasuko Rikihisa
author_facet Rory C. Chien
Lin Mingqun
Qi Yan
Nina Randolph
Weiyan Huang
Maxey Wellman
Ramiro Toribio
Yasuko Rikihisa
author_sort Rory C. Chien
collection DOAJ
description ABSTRACT The tick-borne obligatory intracellular bacterium Anaplasma phagocytophilum infects granulocytes of humans as well as domesticated and wild animals, causing a febrile disease collectively called granulocytic anaplasmosis. The host species specificity and zoonotic potential of A. phagocytophilum strains remain unclear. In the USA, human granulocytic anaplasmosis (HGA) is primarily reported in Wisconsin and Minnesota, the northeastern coastal states, and northern California. In horses, A. phagocytophilum causes equine granulocytic anaplasmosis (EGA). Although EGA has been reported in the same US regions as HGA, horses with a definitive diagnosis of EGA have not been reported in Ohio, where the incidence of HGA is low. In this study, samples from archived blood smears or whole blood from three horses from three different counties in Ohio that presented in 2018, 2020, and 2021 with clinical signs and laboratory findings consistent with EGA were evaluated by PCR and sequencing. Sequences of ankA (encoding ankyrin A) of the three A. phagocytophilum strains were identical and related to strains isolated from humans in the northeastern USA yet distinct from those in California or Europe based on phylogenetic analysis. Each Ohio strain contains unique A. phagocytophilum p44 genes encoding the immunodominant major outer membrane proteins, underscoring the antigenic diversity of A. phagocytophilum strains that cause EGA in Ohio. From 2018 to 2023, 14 additional cases of EGA were identified by serodiagnosis in Ohio and nearby locations in Pennsylvania, pointing to a heretofore unrecognized prevalence of EGA and the risk of transmission of anaplasmosis to humans and animals in this region. IMPORTANCE The tick-borne obligatory intracellular bacterium Anaplasma phagocytophilum infects humans as well as domesticated and wild animals, causing a febrile disease collectively called granulocytic anaplasmosis. The epidemiology and the host species specificity and zoonotic potential of A. phagocytophilum strains remain unclear. In this study, ankA (encoding ankyrin A) and p44 gene sequences of A. phagocytophilum were determined in clinical specimens from horses in Ohio and compared with those found in A. phagocytophilum strains from various hosts and geographic regions. With increasing numbers of seropositive horses, the study points out the unrecognized prevalence and uncharacterized strains of A. phagocytophilum infection in horses and the importance of A. phagocytophilum molecular testing for the prevention of equine and human granulocytic anaplasmosis.
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spelling doaj.art-54d8316b525748389e9de22d609265462023-12-12T13:17:19ZengAmerican Society for MicrobiologyMicrobiology Spectrum2165-04972023-12-0111610.1128/spectrum.02632-23Strains of Anaplasma phagocytophilum from horses in Ohio are related to isolates from humans in the northeastern USARory C. Chien0Lin Mingqun1Qi Yan2Nina Randolph3Weiyan Huang4Maxey Wellman5Ramiro Toribio6Yasuko Rikihisa7Laboratory of Molecular, Cellular, and Environmental Rickettsiology, Infectious Diseases Institute, The Ohio State University , Columbus, Ohio, USALaboratory of Molecular, Cellular, and Environmental Rickettsiology, Infectious Diseases Institute, The Ohio State University , Columbus, Ohio, USALaboratory of Molecular, Cellular, and Environmental Rickettsiology, Infectious Diseases Institute, The Ohio State University , Columbus, Ohio, USADepartment of Veterinary Biosciences, College of Veterinary Medicine, The Ohio State University , Columbus, Ohio, USALaboratory of Molecular, Cellular, and Environmental Rickettsiology, Infectious Diseases Institute, The Ohio State University , Columbus, Ohio, USADepartment of Veterinary Biosciences, College of Veterinary Medicine, The Ohio State University , Columbus, Ohio, USADepartment of Veterinary Clinical Sciences, College of Veterinary Medicine, The Ohio State University , Columbus, Ohio, USALaboratory of Molecular, Cellular, and Environmental Rickettsiology, Infectious Diseases Institute, The Ohio State University , Columbus, Ohio, USAABSTRACT The tick-borne obligatory intracellular bacterium Anaplasma phagocytophilum infects granulocytes of humans as well as domesticated and wild animals, causing a febrile disease collectively called granulocytic anaplasmosis. The host species specificity and zoonotic potential of A. phagocytophilum strains remain unclear. In the USA, human granulocytic anaplasmosis (HGA) is primarily reported in Wisconsin and Minnesota, the northeastern coastal states, and northern California. In horses, A. phagocytophilum causes equine granulocytic anaplasmosis (EGA). Although EGA has been reported in the same US regions as HGA, horses with a definitive diagnosis of EGA have not been reported in Ohio, where the incidence of HGA is low. In this study, samples from archived blood smears or whole blood from three horses from three different counties in Ohio that presented in 2018, 2020, and 2021 with clinical signs and laboratory findings consistent with EGA were evaluated by PCR and sequencing. Sequences of ankA (encoding ankyrin A) of the three A. phagocytophilum strains were identical and related to strains isolated from humans in the northeastern USA yet distinct from those in California or Europe based on phylogenetic analysis. Each Ohio strain contains unique A. phagocytophilum p44 genes encoding the immunodominant major outer membrane proteins, underscoring the antigenic diversity of A. phagocytophilum strains that cause EGA in Ohio. From 2018 to 2023, 14 additional cases of EGA were identified by serodiagnosis in Ohio and nearby locations in Pennsylvania, pointing to a heretofore unrecognized prevalence of EGA and the risk of transmission of anaplasmosis to humans and animals in this region. IMPORTANCE The tick-borne obligatory intracellular bacterium Anaplasma phagocytophilum infects humans as well as domesticated and wild animals, causing a febrile disease collectively called granulocytic anaplasmosis. The epidemiology and the host species specificity and zoonotic potential of A. phagocytophilum strains remain unclear. In this study, ankA (encoding ankyrin A) and p44 gene sequences of A. phagocytophilum were determined in clinical specimens from horses in Ohio and compared with those found in A. phagocytophilum strains from various hosts and geographic regions. With increasing numbers of seropositive horses, the study points out the unrecognized prevalence and uncharacterized strains of A. phagocytophilum infection in horses and the importance of A. phagocytophilum molecular testing for the prevention of equine and human granulocytic anaplasmosis.https://journals.asm.org/doi/10.1128/spectrum.02632-23Anaplasma phagocytophilumhorsesankAp44equine granulocytic anaplasmosis
spellingShingle Rory C. Chien
Lin Mingqun
Qi Yan
Nina Randolph
Weiyan Huang
Maxey Wellman
Ramiro Toribio
Yasuko Rikihisa
Strains of Anaplasma phagocytophilum from horses in Ohio are related to isolates from humans in the northeastern USA
Microbiology Spectrum
Anaplasma phagocytophilum
horses
ankA
p44
equine granulocytic anaplasmosis
title Strains of Anaplasma phagocytophilum from horses in Ohio are related to isolates from humans in the northeastern USA
title_full Strains of Anaplasma phagocytophilum from horses in Ohio are related to isolates from humans in the northeastern USA
title_fullStr Strains of Anaplasma phagocytophilum from horses in Ohio are related to isolates from humans in the northeastern USA
title_full_unstemmed Strains of Anaplasma phagocytophilum from horses in Ohio are related to isolates from humans in the northeastern USA
title_short Strains of Anaplasma phagocytophilum from horses in Ohio are related to isolates from humans in the northeastern USA
title_sort strains of anaplasma phagocytophilum from horses in ohio are related to isolates from humans in the northeastern usa
topic Anaplasma phagocytophilum
horses
ankA
p44
equine granulocytic anaplasmosis
url https://journals.asm.org/doi/10.1128/spectrum.02632-23
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