Tick-borne pathogens detected in sheltered dogs during an epidemic of Rocky Mountain spotted fever, a One Health challenge

Laura Backus Department of Veterinary Medicine and Epidemiology, School of Veterinary Medicine, University of California-Davis, Davis, CA

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Janet Foley Department of Veterinary Medicine and Epidemiology, School of Veterinary Medicine, University of California-Davis, Davis, CA

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Claire Chung Department of Veterinary Medicine and Epidemiology, School of Veterinary Medicine, University of California-Davis, Davis, CA

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Sophia Virata Department of Veterinary Medicine and Epidemiology, School of Veterinary Medicine, University of California-Davis, Davis, CA

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Oscar E. Zazueta Departamento Estatal de Epidemiología, Instituto de Servicios de Salud Pública del Estado de Baja California, Mexicali, México

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Andrés López-Pérez Department of Veterinary Medicine and Epidemiology, School of Veterinary Medicine, University of California-Davis, Davis, CA

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Abstract

OBJECTIVE

To assess exposure to and infection with 3 pathogens (Rickettsia rickettsii, Anaplasma platys, and Ehrlichia canis) vectored by brown dog ticks (Rhipicephalus sanguineus) in sheltered dogs at the western US–Mexico border.

ANIMALS

239 dogs in shelters in San Diego and Imperial counties, US, and Mexicali and Tijuana, Mexico.

PROCEDURES

Each dog had blood drawn and basic demographic data collected. PCR was performed to determine active infection with Rickettsia spp, E canis, and A platys. Serology was performed to determine exposure to Rickettsia, Anaplasma, and Ehrlichia species.

RESULTS

2 of 78 (2.6%) dogs sampled in Tijuana were actively infected with R rickettsii. A single brown dog tick collected from a dog in Tijuana was PCR-positive for R rickettsii. Infection with E canis and A platys ranged across shelters from 0% to 27% and 0% to 33%, respectively. Dogs in all 4 locations demonstrated exposure to all 3 pathogens, though Rickettsia and Ehrlichia seropositivity was highest in Mexicali (81% and 49%, respectively) and Anaplasma seropositivity was highest in Tijuana (45%).

CLINICAL RELEVANCE

While infection and exposure were highest in sheltered dogs in the southern locations, dogs in all locations demonstrated exposure to all pathogens, demonstrating the potential for emergence and spread of zoonotic pathogens with significant public health consequences in southern California and northern Baja California. In addition, veterinarians and shelter staff should be aware that Ehrlichia or Anaplasma infection may co-occur with Rocky Mountain spotted fever, which is a human health risk.

Abstract

OBJECTIVE

To assess exposure to and infection with 3 pathogens (Rickettsia rickettsii, Anaplasma platys, and Ehrlichia canis) vectored by brown dog ticks (Rhipicephalus sanguineus) in sheltered dogs at the western US–Mexico border.

ANIMALS

239 dogs in shelters in San Diego and Imperial counties, US, and Mexicali and Tijuana, Mexico.

PROCEDURES

Each dog had blood drawn and basic demographic data collected. PCR was performed to determine active infection with Rickettsia spp, E canis, and A platys. Serology was performed to determine exposure to Rickettsia, Anaplasma, and Ehrlichia species.

RESULTS

2 of 78 (2.6%) dogs sampled in Tijuana were actively infected with R rickettsii. A single brown dog tick collected from a dog in Tijuana was PCR-positive for R rickettsii. Infection with E canis and A platys ranged across shelters from 0% to 27% and 0% to 33%, respectively. Dogs in all 4 locations demonstrated exposure to all 3 pathogens, though Rickettsia and Ehrlichia seropositivity was highest in Mexicali (81% and 49%, respectively) and Anaplasma seropositivity was highest in Tijuana (45%).

CLINICAL RELEVANCE

While infection and exposure were highest in sheltered dogs in the southern locations, dogs in all locations demonstrated exposure to all pathogens, demonstrating the potential for emergence and spread of zoonotic pathogens with significant public health consequences in southern California and northern Baja California. In addition, veterinarians and shelter staff should be aware that Ehrlichia or Anaplasma infection may co-occur with Rocky Mountain spotted fever, which is a human health risk.

  • 1.

    Dantas-Torres F, Otranto D. Best practices for preventing vector-borne diseases in dogs and humans. Trends Parasitol. 2016;32(1):4355. doi:10.1016/j.pt.2015.09.004

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 2.

    Alvarez-Hernandez G, Drexler N, Paddock CD, et al. Community-based prevention of epidemic Rocky Mountain spotted fever among minority populations in Sonora, Mexico, using a One Health approach. Trans R Soc Trop Med Hyg. 2020;114(4):293300. doi:10.1093/trstmh/trz114

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 3.

    Halliday JEB, Meredith AL, Knobel DL, Shaw DJ, Bronsvoort BM, Cleaveland S. A framework for evaluating animals as sentinels for infectious disease surveillance. J R Soc Interface. 2007;4(16):973984. doi:10.1098/rsif.2007.0237

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 4.

    Dantas-Torres F. Biology and ecology of the brown dog tick, Rhipicephalus sanguineus. Parasit Vectors. 2010;3(1):26 doi:10.1186/1756-3305-3-26

  • 5.

    Demma LJ, Traeger MS, Nicholson WL, et al. Rocky Mountain spotted fever from an unexpected tick vector in Arizona. N Engl J Med. 2005;353(6):587594. doi:10.1056/NEJMoa050043

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 6.

    Dumler JS, Barbet AF, Bekker CP, et al. Reorganization of genera in the families Rickettsiaceae and Anaplasmataceae in the order Rickettsiales: unification of some species of Ehrlichia with Anaplasma, Cowdria with Ehrlichia and Ehrlichia with Neorickettsia, descriptions of six new species combinations and designation of Ehrlichia equi and ‘HGE agent’ as subjective synonyms of Ehrlichia phagocytophila. Int J Syst Evol Microbiol. 2001;51(Pt 6):21452165. doi:10.1099/00207713-51-6-2145

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 7.

    Shpynov SN, Fournier P-E, Pozdnichenko NN, Gumenuk AS, Skiba AA. New approaches in the systematics of rickettsiae. New Microbes New Infect. 2018;23:93102. doi:10.1016/j.nmni.2018.02.012

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 8.

    Eremeeva ME, Dasch GA. Challenges posed by tick-borne rickettsiae: eco-epidemiology and public health implications. Front Public Health. Published online April 21, 2020. doi:10.3389/fpubh.2015.00055

    • Search Google Scholar
    • Export Citation
  • 9.

    Levin ML, Killmaster LF, Zemtsova GE, Ritter JM, Langham G. Clinical presentation, convalescence, and relapse of rocky mountain spotted fever in dogs experimentally infected via tick bite. PLoS One. 2014;9(12):e115105 doi:10.1371/journal.pone.0115105

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 10.

    Biggs HM, Behravesh CB, Bradley KK, et al. Diagnosis and management of tickborne rickettsial diseases: Rocky Mountain spotted fever and other spotted fever group rickettsioses, ehrlichioses, and anaplasmosis—United States: a practical guide for health care and public health professionals. MMWR Recomm Rep. 2016;65(2):144. doi:10.15585/mmwr.rr6502a1

    • Search Google Scholar
    • Export Citation
  • 11.

    Álvarez-López DI, Ochoa-Mora E, Nichols Heitman K, Binder AM, Álvarez-Hernández G, Armstrong PA. Epidemiology and clinical features of Rocky Mountain spotted fever from enhanced surveillance, Sonora, Mexico: 2015–2018. Am J Trop Med Hyg. 2021;104(1):190197. doi:10.4269/ajtmh.20-0854

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 12.

    Foley J, Tinoco-Gracia L, Rodriguez-Lomelí M, et al. Unbiased assessment of abundance of Rhipicephalus sanguineus sensu lato ticks, canine exposure to spotted fever group rickettsia, and risk factors in Mexicali, México. Am J Trop Med Hyg. 2019;101(1):2232. doi:10.4269/ajtmh.18-0878

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 13.

    Pieracci EG, Rosa JDPDL, Rubio DL, et al. Seroprevalence of spotted fever group rickettsiae in canines along the United States–Mexico border. Zoonoses Public Health 2019;0. Accessed Aug 27, 2019. onlinelibrary.wiley.com/doi/abs/10.1111/zph.12642

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 14.

    Yaglom HD, Nicholson WL, Casal M, Nieto NC, Adams L. Serologic assessment for exposure to spotted fever group rickettsiae in dogs in the Arizona-Sonora border region. Zoonoses Public Health. 2018;65(8):984992. doi:10.1111/zph.12517

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 15.

    López-Pérez AM, Orozco L, Zazueta OE, Fierro M, Gomez P, Foley J. An exploratory analysis of demography and movement patterns of dogs: new insights in the ecology of endemic Rocky Mountain-Spotted Fever in Mexicali, Mexico. PLoS One. 2020;15(5):e0233567. doi:10.1371/journal.pone.0233567

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 16.

    Parola P, Socolovschi C, Jeanjean L, et al. Warmer weather linked to tick attack and emergence of severe rickettsioses. PLoS Negl Trop Dis. 2008;2(11):e338. doi:10.1371/journal.pntd.0000338

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 17.

    Nava S, Beati L, Venzal JM, et al. Rhipicephalus sanguineus (Latreille, 1806): neotype designation, morphological re-description of all parasitic stages and molecular characterization. Ticks Tick Borne Dis. 2018;9(6):15731585. doi:10.1016/j.ttbdis.2018.08.001

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 18.

    Bremer WG, Schaefer JJ, Wagner ER, et al. Transstadial and intrastadial experimental transmission of Ehrlichia canis by male Rhipicephalus sanguineus. Vet Parasitol. 2005;131(1–2):95105. doi:10.1016/j.vetpar.2005.04.030

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 19.

    Snellgrove AN, Krapiunaya I, Ford SL, et al. Vector competence of Rhipicephalus sanguineus sensu stricto for Anaplasma platys. Ticks Tick Borne Dis. 2020;11(6):101517. doi:10.1016/j.ttbdis.2020.101517

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 20.

    Eremeeva ME, Bosserman EA, Demma LJ, Zambrano ML, Blau DM, Dasch GA. Isolation and identification of Rickettsia massiliae from Rhipicephalus sanguineus ticks collected in Arizona. Appl Environ Microbiol. 2006;72(8):55695577. doi:10.1128/AEM.00122-06

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 21.

    Arraga-Alvarado CM, Qurollo BA, Parra OC, Berrueta MA, Hegarty BC, Breitschwerdt EB. Case report: molecular evidence of Anaplasma platys infection in two women from Venezuela. Am J Trop Med Hyg. 2014;91(6):11611165. doi:10.4269/ajtmh.14-0372

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 22.

    Maggi RG, Mascarelli PE, Havenga LN, Naidoo V, Breitschwerdt EB. Co-infection with Anaplasma platys, Bartonella henselae and Candidatus Mycoplasma haematoparvum in a veterinarian. Parasit Vectors. 2013;6(1):103. doi:10.1186/1756-3305-6-103

    • Search Google Scholar
    • Export Citation
  • 23.

    Diniz PPVP, Beall MJ, Omark K, et al. High prevalence of tick-borne pathogens in dogs from an Indian reservation in northeastern Arizona. Vector Borne Zoonotic Dis. 2010;10(2):117123. doi:10.1089/vbz.2008.0184

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 24.

    Greene C. Infectious Diseases of the Dog and Cat. 4th ed. Elsevier; 2012.

  • 25.

    Burton W, Drake C, Ogeer J, et al. Association between exposure to Ehrlichia spp. and risk of developing chronic kidney disease in dogs. J Am Anim Hosp Assoc. 2020;56(3):159164. doi:10.5326/JAAHA-MS-7012

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 26.

    Gaunt S, Beall M, Stillman B, et al. Experimental infection and co-infection of dogs with Anaplasma platys and Ehrlichia canis: hematologic, serologic and molecular findings. Parasit Vectors. 2010;3(1):33. doi:10.1186/1756-3305-3-33

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 27.

    Lanza-Perea M, Zieger U, Qurollo BA, et al. Intraoperative bleeding in dogs from Grenada seroreactive to Anaplasma platys and Ehrlichia canis. J Vet Intern Med. 2014;28(6):17021707. doi:10.1111/jvim.12442

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 28.

    Kidd L, Qurollo B, Lappin M, et al. Prevalence of vector-borne pathogens in Southern California dogs with clinical and laboratory abnormalities consistent with immune-mediated disease. J Vet Intern Med. 2017;31(4):10811090. doi:10.1111/jvim.14735

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 29.

    Herrick KL, Pena SA, Yaglom HD, et al. Rickettsia parkeri Rickettsiosis, Arizona, USA. Emerg Infect Dis. 2016;22(5):780785. doi:10.3201/eid2205.151824

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 30.

    Zazueta OE, Armstrong PA, Márquez-Elguea A, et al. Rocky Mountain spotted fever in a large metropolitan center, Mexico–United States border, 2009–2019. Emerg Infect Dis. 2021;27(6):15671576. doi:10.3201/eid2706.191662

    • Search Google Scholar
    • Export Citation
  • 31.

    Otranto D, Dantas-Torres F, Mihalca AD, Traub RJ, Lappin M, Baneth G. Zoonotic parasites of sheltered and stray dogs in the era of the global economic and political crisis. Trends Parasitol. 2017;33(10):813825. doi:10.1016/j.pt.2017.05.013

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 32.

    Wright I, Jongejan F, Marcondes M, et al. Parasites and vector-borne diseases disseminated by rehomed dogs. Parasit Vectors. 2020;13(1):546. doi:10.1186/s13071-020-04407-5

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 33.

    Estrada I, Balagot C, Fierro M, et al. Spotted fever group rickettsiae canine serosurveillance near the US-Mexico border in California. Zoonoses Public Health. 2020;67(2):148155. doi:10.1111/zph.12666

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 34.

    Eastland-Jones RC, German AJ, Holden SL, Biourge V, Pickavance LC. Owner misperception of canine body condition persists despite use of a body condition score chart. J Nutr Sci. 2014;3:e45. doi:10.1017/jns.2014.25.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 35.

    Furman DP, Loomis EC. The Ticks of California (Acari:Ixodida). University of California Press; 1984.

  • 36.

    Stenos J, Graves SR, Unsworth NB. A highly sensitive and specific real-time PCR assay for the detection of spotted fever and typhus group Rickettsiae. Am J Trop Med Hyg. 2005;73(6):10831085. doi:10.4269/ajtmh.2005.73.1083

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 37.

    Kato CY, Chung IH, Robinson LK, Austin AL, Dasch GA, Massung RF. Assessment of real-time PCR assay for detection of Rickettsia spp. and Rickettsia rickettsii in banked clinical samples. J Clin Microbiol. 2013;51(1):314317. doi:10.1128/JCM.01723-12

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 38.

    Doyle CK, Labruna MB, Breitschwerdt EB, et al. Detection of medically important Ehrlichia by quantitative multicolor TaqMan real-time polymerase chain reaction of the dsb gene. J Mol Diagn. 2005;7(4):504510. doi:10.1016/S1525-1578(10)60581-8

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 39.

    Shapiro MR, Fritz CL, Tait K, et al. Rickettsia 364D: a newly recognized cause of eschar-associated illness in California. Clin Infect Dis. 2010;50(4):541548. doi:10.1086/649926

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 40.

    Roux V, Fournier PE, Raoult D. Differentiation of spotted fever group rickettsiae by sequencing and analysis of restriction fragment length polymorphism of PCR-amplified DNA of the gene encoding the protein rOmpA. J Clin Microbiol. 1996;34(9):20582065. doi:10.1128/jcm.34.9.2058-2065.1996

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 41.

    Fournier PE, Dumler JS, Greub G, Zhang J, Wu Y, Raoult D. Gene sequence-based criteria for identification of new rickettsia isolates and description of Rickettsia heilongjiangensis sp. nov. J Clin Microbiol. 2003;41(12):54565465. doi:10.1128/JCM.41.12.5456-5465.2003

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 42.

    Renvoisé A, Rolain J-M, Socolovschi C, Raoult D. Widespread use of real-time PCR for rickettsial diagnosis. FEMS Immunol Med Microbiol. 2012;64(1):126129. doi:10.1111/j.1574-695X.2011.00899.x

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 43.

    Raoult D, Paddock CD. Rickettsia parkeri infection and other spotted fevers in the United States. N Engl J Med. 2005;353(6):626627. doi:10.1056/NEJM200508113530617

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 44.

    Angelakis E, Mediannikov O, Parola P, Raoult D. Rickettsia felis: the complex journey of an emergent human pathogen. Trends Parasitol. 2016;32(7):554564. doi:10.1016/j.pt.2016.04.009

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 45.

    de Oliveira JCP, Reckziegel GH, Ramos CADN, et al. Detection of Rickettsia felis in ectoparasites collected from domestic animals. Exp Appl Acarol. 2020;81(2):255264. doi:10.1007/s10493-020-00505-2

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 46.

    Beeler E, Abramowicz KF, Zambrano ML, et al. A focus of dogs and Rickettsia massiliae-infected Rhipicephalus sanguineus in California. Am J Trop Med Hyg. 2011;84(2):244249. doi:10.4269/ajtmh.2011.10-0355

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 47.

    López-Pérez AM, Chaves A, Sánchez-Montes S, et al. Diversity of rickettsiae in domestic, synanthropic, and sylvatic mammals and their ectoparasites in a spotted fever-epidemic region at the western US-Mexico border. Transbound Emerg Dis. 2022;69(2):609622. doi:10.1111/tbed.14027

    • Search Google Scholar
    • Export Citation
  • 48.

    Yamane I, Gardner IA, Ryan CP, Levy M, Urrico J, Conrad PA. Serosurvey of Babesia canis, Babesia gibsoni and Ehrlichia canis in pound dogs in California, USA. Prev Vet Med. 1994;18(4):293304. doi:10.1016/0167-5877(94)90054-X

    • Search Google Scholar
    • Export Citation
  • 49.

    Almazán C, González-Álvarez VH, Fernández de Mera IG, Cabezas-Cruz A, Rodríguez-Martínez R, de la Fuente J. Molecular identification and characterization of Anaplasma platys and Ehrlichia canis in dogs in Mexico. Ticks Tick Borne Dis. 2016;7(2):276283. doi:10.1016/j.ttbdis.2015.11.002

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 50.

    Companion Animal Parasite Council. Parasite Prevalence Maps. Parasite Preval Maps 2022. Accessed July 16, 2022. capcvet.org/maps/

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