Volume 101, Issue 6
  • ISSN: 0002-9637
  • E-ISSN: 1476-1645



Human granulocytic anaplasmosis (HGA), caused by the bacteria , is transmitted to humans by blacklegged ticks () in eastern North America. To assess the emergence of . in Ontario, we analyzed patient serological and clinical data in combination with pathogen detection in blacklegged ticks from 2011 to 2017. Our sample population included all patients who had serological testing ordered by their physicians ( = 851). Eighty-three patients (10.8%) were . seropositive (IgG titers ≥ 1:64) and 686 (89.2%) were seronegative (IgG titers < 1:64). Applying published surveillance case definitions, we classified zero as confirmed, five as probable, and 78 as suspected cases. The percentage of seropositive patients remained generally stable at 13.6%. Seropositive patients were most often adult females, 40–59 years of age, and reported nonspecific signs and symptoms, such as fatigue, headache, and fever. Higher seropositivity rates (≥ 1.5 patients per 100,000 population) occurred in eastern and northwestern Ontario. The percentage of . -positive blacklegged ticks, through passive and active surveillance, was 0.4 and 1.1%, respectively, and increased over time. Serological and entomological indicators of . activity increased in areas of the province with established blacklegged tick populations. The risk of HGA is presently low in Ontario; however, further research is required to document the epidemiology of HGA in the province. To minimize the impact of HGA emergence in Ontario, increased awareness and education of the public and health-care providers is recommended, with consideration to making HGA a reportable infection in Ontario.

[open-access] This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.


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  1. Weil AA, Baron EL, Brown CM, Drapkin MS, , 2012. Clinical findings and diagnosis in human granulocytic anaplasmosis: a case series from Massachusetts. Mayo Clin Proc 87: 233239. [Google Scholar]
  2. Bakken JS, Dumler JS, , 2015. Human granulocytic anaplasmosis. Infect Dis Clin North Am 29: 341355. [Google Scholar]
  3. Dumler JS, Choi KS, Garcia-Garcia JC, Barat NS, Scorpio DG, Garyu JW, Grab DJ, Bakken JS, , 2005. Human granulocytic anaplasmosis and Anaplasma phagocytophilum. Emerg Infect Dis 11: 18281834. [Google Scholar]
  4. Dumler JS, Madigan JE, Pusterla N, Bakken JS, , 2007. Ehrlichioses in humans: epidemiology, clinical presentation, diagnosis, and treatment. Clin Infect Dis 45 (Suppl 1): S45S51. [Google Scholar]
  5. Dahlgren FS, Mandel EJ, Krebs JW, Massung RF, McQuiston JH, , 2011. Increasing incidence of Ehrlichia chaffeensis and Anaplasma phagocytophilum in the United States, 2000–2007. Am J Trop Med Hyg 85: 124131. [Google Scholar]
  6. Dahlgren FS, Heitman KN, Drexler NA, Massung RF, Behravesh CB, , 2015. Human granulocytic anaplasmosis in the United States from 2008 to 2012: a summary of national surveillance data. Am J Trop Med Hyg 93: 6672. [Google Scholar]
  7. Chapman AS, 2006. Diagnosis and management of tickborne rickettsial diseases: rocky Mountain spotted fever, ehrlichioses, and anaplasmosis–United States: a practical guide for physicians and other health-care and public health professionals. MMWR Recomm Rep 55: 127. [Google Scholar]
  8. Annen K, Friedman K, Eshoa C, Horowitz M, Gottschall J, Straus T, , 2012. Two cases of transfusion-transmitted Anaplasma phagocytophilum. Am J Clin Pathol 137: 562565. [Google Scholar]
  9. Horowitz HW, Kilchevsky E, Haber S, Aguero-Rosenfeld M, Kranwinkel R, James EK, Wong SJ, Chu F, Liveris D, Schwartz I, , 1998. Perinatal transmission of the agent of human granulocytic ehrlichiosis. N Engl J Med 339: 375378. [Google Scholar]
  10. Bakken JS, Krueth JK, Lund T, Malkovitch D, Asanovich K, Dumler JS, , 1996. Exposure to deer blood may be a cause of human granulocytic ehrlichiosis. Clin Infect Dis 23: 198. [Google Scholar]
  11. Keesing F, McHenry DJ, Hersh M, Tibbetts M, Brunner JL, Killilea M, LoGiudice K, Schmidt KA, Ostfeld RS, , 2014. Prevalence of human-active and variant 1 strains of the tick-borne pathogen Anaplasma phagocytophilum in hosts and forests of eastern North America. Am J Trop Med Hyg 91: 302309. [Google Scholar]
  12. Keesing F, Hersh M, Tibbetts M, McHenry D, Duerr S, Brunner J, Killilea M, LoGiudice K, Schmidt K, Ostfeld R, , 2012. Reservoir competence of vertebrate hosts for Anaplasma phagocytophilum. Emerg Infect Dis 18: 20132016. [Google Scholar]
  13. Telford SR, 3rd Dawson JE, Katavolos P, Warner CK, Kolbert CP, Persing DH, , 1996. Perpetuation of the agent of human granulocytic ehrlichiosis in a deer tick-rodent cycle. Proc Natl Acad Sci USA 93: 62096214. [Google Scholar]
  14. Trost CN, Lindsay LR, Dibernardo A, Chilton NB, , 2018. Three genetically distinct clades of Anaplasma phagocytophilum in Ixodes scapularis. Ticks Tick Borne Dis 9: 15181527. [Google Scholar]
  15. Krakowetz CN, Dibernardo A, Lindsay LR, Chilton NB, , 2014. Two Anaplasma phagocytophilum strains in Ixodes scapularis ticks, Canada. Emerg Infect Dis 20: 20642067. [Google Scholar]
  16. Massung RF, Mauel MJ, Owens JH, Allan N, Courtney JW, Stafford KC, Mather TN, , 2002. Genetic variants of Ehrlichia phagocytophila, Rhode Island and Connecticut. Emerg Infect Dis 8: 467472. [Google Scholar]
  17. Massung RF, Courtney JW, Hiratzka SL, Pitzer VE, Smith G, Dryden RL, , 2005. Anaplasma phagocytophilum in white-tailed deer. Emerg Infect Dis 11: 16041606. [Google Scholar]
  18. Massung RF, Mather TN, Priestley RA, Levin ML, , 2003. Transmission efficiency of the AP-variant 1 strain of Anaplasma phagocytophila. Ann N Y Acad Sci 990: 7579. [Google Scholar]
  19. Lovrich SD, Jobe DA, Kowalski TJ, Policepatil SM, Callister SM, , 2011. Expansion of the Midwestern focus for human granulocytic anaplasmosis into the region surrounding La Crosse, Wisconsin. J Clin Microbiol 49: 38553859. [Google Scholar]
  20. Bakken JS, 1998. Seroprevalence of human granulocytic ehrlichiosis among permanent residents of northwestern Wisconsin. Clin Infect Dis 27: 14911496. [Google Scholar]
  21. Aguero-Rosenfeld ME, Donnarumma L, Zentmaier L, Jacob J, Frey M, Noto R, Carbonaro CA, Wormser GP, , 2002. Seroprevalence of antibodies that react with Anaplasma phagocytophila, the agent of human granulocytic ehrlichiosis, in different populations in Westchester county, New York. J Clin Microbiol 40: 26122615. [Google Scholar]
  22. Clow KM, Ogden NH, Lindsay LR, Michel P, Pearl DL, Jardine CM, , 2016. Distribution of ticks and the risk of Lyme disease and other tick–borne pathogens of public health significance in Ontario, Canada. Vector Borne Zoonotic Dis 16: 215222. [Google Scholar]
  23. Nelder MP, Russell C, Lindsay LR, Dhar B, Patel SN, Johnson S, Moore S, Kristjanson E, Li Y, Ralevski F, , 2014. Population-based passive tick surveillance and detection of expanding foci of blacklegged ticks Ixodes scapularis and the Lyme disease agent Borrelia burgdorferi in Ontario, Canada. PLoS One 9: e105358. [Google Scholar]
  24. Johnson KO, Nelder MP, Russell C, Li Y, Badiani T, Sander B, Sider D, Patel SN, , 2018. Clinical manifestations of reported Lyme disease cases in Ontario, Canada: 2005–2014. PLoS One 13: e0198509. [Google Scholar]
  25. Parkins MD, Church DL, Jiang XY, Gregson DB, , 2009. Human granulocytic anaplasmosis: first reported case in Canada. Can J Infect Dis Med Microbiol 20: e100e102. [Google Scholar]
  26. Manitoba Health, Seniors and Active Living, 2018. Tick-Borne Diseases. Winnipeg, Canada: Manitoba Government. Available at: https://www.gov.mb.ca/health/publichealth/cdc/tickborne/index.html. Accessed May 2, 2019. [Google Scholar]
  27. Werden L, Lindsay LR, Barker IK, Bowman J, Gonzales EK, Jardine CM, , 2015. Prevalence of Anaplasma phagocytophilum and Babesia microti in Ixodes scapularis from a newly established Lyme disease endemic area, the Thousand Islands region of Ontario, Canada. Vector Borne Zoonotic Dis 15: 627629. [Google Scholar]
  28. Artsob H, , 1996. Tick-transmitted human disease threats in Canada. Germs Ideas 2: 3539. [Google Scholar]
  29. Edginton S, Guan TH, Evans G, Srivastava S, , 2018. Human granulocytic anaplasmosis acquired from a blacklegged tick in Ontario. CMAJ 190: E363E366. [Google Scholar]
  30. Manitoba Public Health Branch, 2016. Communicable Disease Management Protocol: Anaplasmosis (Human Granulocytic Anaplasmosis). Winnipeg, Canada: Manitoba Public Health Branch. [Google Scholar]
  31. Centers for Disease Control and Prevention (CDC), 2008. Ehrlichiosis and Anaplasmosis: 2008 Case Definition. Atlanta, GA: CDC. Available at: https://wwwn.cdc.gov/nndss/conditions/ehrlichiosis-and-anaplasmosis/case-definition/2008/. Accessed January 11, 2019. [Google Scholar]
  32. Ontario Agency for Health Protection and Promotion (Public Health Ontario), 2016. Blacklegged Tick Surveillance in Ontario: A Systematic Review. Toronto, Canada: Queen’s Printer for Ontario. [Google Scholar]
  33. Stafford KC, Williams SC, Molaei G, , 2017. Integrated pest management in controlling ticks and tick-associated diseases. J Integr Pest Manag 8: 28. [Google Scholar]
  34. Ontario Agency for Health Protection and Promotion (Public Health Ontario), 2017. Ontario Lyme Disease Estimated Risk Areas Map, 2017. Toronto, Canada: Queen’s Printer for Ontario. [Google Scholar]
  35. Ontario Agency for Health Protection and Promotion (Public Health Ontario), 2016. Technical Report: Update on Lyme Disease Prevention and Control. Toronto, Canada: Queen’s Printer for Ontario. [Google Scholar]
  36. Ogden NHK, Koffi JK, Lindsay LR, , 2014. Assessment of a screening test to identify Lyme disease risk. Can Commun Dis Rep 40: 8387. [Google Scholar]
  37. Dibernardo A, Cote T, Ogden NH, Lindsay LR, , 2014. The prevalence of Borrelia miyamotoi infection, and co-infections with other Borrelia spp. in Ixodes scapularis ticks collected in Canada. Parasit Vectors 7: 183. [Google Scholar]
  38. Schillberg E, Lunny D, Lindsay LR, Nelder MP, Russell C, Mackie M, Coats D, Berry A, Young Hoon KN, , 2018. Distribution of Ixodes scapularis in northwestern Ontario: results from active and passive surveillance activities in the Northwestern Health Unit catchment area. Int J Environ Res Public Health 15: E2225. [Google Scholar]
  39. Courtney JW, Kostelnik LM, Zeidner NS, Massung RF, , 2004. Multiplex real-time PCR for detection of Anaplasma phagocytophilum and Borrelia burgdorferi. J Clin Microbiol 42: 31643168. [Google Scholar]
  40. Minnesota Department of Health, 2018. Reported Cases of Anaplasmosis in Minnesota by Year, 1996–2017. Saint Paul, MN: Minnesota Department of Health. Available at: https://www.health.state.mn.us/diseases/anaplasmosis/statistics.html. Accessed January 11, 2019. [Google Scholar]
  41. Institut National de Santé Publique du Québec, 2016. Report on Surveillance for Lyme Disease: 2016. Québec, Canada: Institut National de Santé Publique du Québec. [Google Scholar]
  42. Institut National de Santé Publique du Québec, 2015. Surveillance of Lyme Disease and Other Diseases Transmitted by the Ixodes Scapularis Tick: 2014. Québec, Canada: Institut National de Santé Publique du Québec. [Google Scholar]
  43. Eisen RJ, Eisen L, Ogden NH, Beard CB, , 2016. Linkages of weather and climate with Ixodes scapularis and Ixodes pacificus (Acari: Ixodidae), enzootic transmission of Borrelia burgdorferi, and Lyme disease in North America. J Med Entomol 53: 250261. [Google Scholar]
  44. Nelder M, Wijayasri S, Russell C, Johnson K, Marchand-Austin A, Cronin K, Johnson S, Badiani T, Patel S, Sider D, , 2018. The continued rise of Lyme disease in Ontario, Canada: 2017. Can Commun Dis Rep 44: 231236. [Google Scholar]
  45. Qurollo BA, 2014. A serological survey of tick-borne pathogens in dogs in North America and the Caribbean as assessed by Anaplasma phagocytophilum, A. platys, Ehrlichia canis, E. chaffeensis, E. ewingii, and Borrelia burgdorferi species-specific peptides. Infect Ecol Epidemiol 4: 24699. [Google Scholar]
  46. Arroyo L, Furness C, Grossenbacher C, Hazlett M, Hunnisett D, McKee M, Moore A, Peatling J, , 2015. A Disease Bulletin from the Equine Network. Avaialble at: https://www.wormsandgermsblog.com/files/2015/11/equine-anaplasmosis-final.pdf. Accessed January 12, 2019. [Google Scholar]
  47. Ogden NH, Maarouf A, Barker IK, Bigras-Poulin M, Lindsay LR, Morshed MG, O'Callaghan CJ, Ramay F, Waltner-Toews D, Charron DF, , 2006. Climate change and the potential for range expansion of the Lyme disease vector Ixodes scapularis in Canada. Int J Parasitol 36: 6370. [Google Scholar]
  48. Ogden NH, 2008. Risk maps for range expansion of the Lyme disease vector, Ixodes scapularis, in Canada now and with climate change. Int J Health Geogr 7: 24. [Google Scholar]
  49. Clow KM, Leighton PA, Ogden NH, Lindsay LR, Michel P, Pearl DL, Jardine CM, , 2017. Northward range expansion of Ixodes scapularis evident over a short timescale in Ontario, Canada. PLoS One 12: e0189393. [Google Scholar]
  50. Neelakanta G, Sultana H, Fish D, Anderson JF, Fikrig E, , 2010. Anaplasma phagocytophilum induces Ixodes scapularis ticks to express an antifreeze glycoprotein gene that enhances their survival in the cold. J Clin Invest 120: 31793190. [Google Scholar]
  51. Ogden NH, 2008. Role of migratory birds in introduction and range expansion of Ixodes scapularis ticks and of Borrelia burgdorferi and Anaplasma phagocytophilum in Canada. Appl Environ Microbiol 74: 17801790. [Google Scholar]
  52. Bakken JS, Haller I, Riddell D, Walls JJ, Dumler JS, , 2002. The serological response of patients infected with the agent of human granulocytic ehrlichiosis. Clin Infect Dis 34: 2227. [Google Scholar]

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Supplemental table

  • Received : 26 Feb 2019
  • Accepted : 16 Jul 2019
  • Published online : 14 Oct 2019

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