Canine infection with Dirofilaria immitis, Borrelia burgdorferi, Anaplasma spp., and Ehrlichia spp. in the United States, 2010–2012

Particle and Fibre Toxicology

John Stamaris²  Ramaswamy Chandrashekar²  Dwight D Bowman¹  Melissa J Beall²  Susan E Little³ 

[1] Department of Microbiology and Immunology, College of Veterinary Medicine, Cornell University, Ithaca, NY, USA;IDEXX Laboratories, Inc., Westbrook, ME, USA;Department of Veterinary Pathobiology, Center for Veterinary Health Sciences, Oklahoma State University, Room 250 McElroy Hall, Stillwater, OK 74078, USA

关键词: Ehrlichia;    Dirofilaria immitis;    Canine;    Borrelia burgdorferi;    Anaplasma;   

Others  :  804641
DOI  :  10.1186/1756-3305-7-257

 received in 2014-03-06, accepted in 2014-05-24,  发布年份 2014

【 摘 要 】

Background

The geographic distribution of canine infection with vector-borne disease agents in the United States appears to be expanding.

Methods

To provide an updated assessment of geographic trends in canine infection with Dirofilaria immitis, Borrelia burgdorferi, Ehrlichia spp., and Anaplasma spp., we evaluated results from an average of 3,588,477 dogs tested annually by veterinarians throughout the United States from 2010 – 2012.

Results

As in an earlier summary report, the percent positive test results varied by agent and region, with antigen of D. immitis and antibody to Ehrlichia spp. most commonly identified in the Southeast (2.9% and 3.2%, respectively) and antibody to both B. burgdorferi and Anaplasma spp. most commonly identified in the Northeast (13.3% and 7.1%, respectively) and upper Midwest (4.4% and 3.9%, respectively). Percent positive test results for D. immitis antigen were lower in every region considered, including in the Southeast, than previously reported. Percent positive test results for antibodies to B. burgdorferi and Ehrlichia spp. were higher nationally than previously reported, and, for antibodies to Anaplasma spp., were higher in the Northeast but lower in the Midwest and West, than in the initial report. Annual reports of human cases of Lyme disease, ehrlichiosis, and anaplasmosis were associated with percent positive canine test results by state for each respective tick-borne disease agent (R² = 0.701, 0.457, and 0.314, respectively). Within endemic areas, percent positive test results for all three tick-borne agents demonstrated evidence of geographic expansion.

Conclusions

Continued national monitoring of canine test results for vector-borne zoonotic agents is an important tool for accurately mapping the geographic distribution of these agents, and greatly aids our understanding of the veterinary and public health threats they pose.

【 授权许可】

   
2014 Little et al.; licensee BioMed Central Ltd.

【 图 表 】

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【 参考文献 】

• [1]Bowman D, Little SE, Lorentzen L, Shields J, Sullivan MP, Carlin EP: Prevalence and geographic distribution of Dirofilaria immitis, Borrelia burgdorferi, Ehrlichia canis, and Anaplasma phagocytophilum in dogs in the United States: results of a national clinic-based serologic survey. Vet Parasitol 2009, 160:138-148.
• [2]Graham W, Rubin SB, Boeckh A, Burhardt LF, Jones S, Miller M, Payne P, Rehm C, Smith-Blackmore M, Stannard R, Nelson CT, Atkins C, Carithers D, McCall J, von Simson C: Current canine guidelines for the diagnosis, prevention, and management of heartworm (Dirofilaria immitis) infection in cats (revised January 2012). http://www.heartwormsociety.org webcite, Accessed October 1, 2013
• [3]Little SE, Heise SR, Blagburn BL, Callister SM, Mead PS: Lyme borreliosis in dogs and people in the USA. Trends Parasitol 2010, 26:213-218.
• [4]Nicholson WL, Allen KE, McQuiston JH, Breitschwerdt EB, Little SE: The increasing recognition of rickettsial pathogens in dogs and people. Trends Parasitol 2010, 26:205-212.
• [5]Companion Animal Parasite Council: CAPC General Guidelines, 2013. http://www.capcvet.org/capc-recommendations/capc-general-guidelines webcite Accessed November 1, 2013
• [6]Hebert D, Eschner A: Seroprevalence of Borrelia burgdorferi-specific C6 antibody in dogs before and after implementation of a nonadjuvanted recombinant outer surface protein A vaccine in a Rhode Island small animal clinic. Vet Ther 2010, 11:E1-E9.
• [7]Gates MC, Nolan TJ: Factors influencing heartworm, flea, and tick preventative use in patients presenting to a veterinary teaching hospital. Prev Vet Med 2010, 93:193-200.
• [8]American Animal Hospital Association (AAHA): AAHA-AVMA canine preventive healthcare guidelines. JAAHA 2011, 47:5.
• [9]Duncan AW, Correa MT, Levine JF, Breitschwerdt EB: The dog as a sentinel for human infection: prevalence of Borrelia burgdorferi C6 antibodies in dogs from southeastern and mid-Atlantic States. Vector Borne Zoonotic Dis 2005, 5:101-109.
• [10]Cardosa L, Mendao C, de Carvalho LM: Prevalence of Dirofilaria immitis, Ehrlichia canis, Borrelia burgdorferi sensu lato, Anaplasma spp. and Leishmania infantum in apparently healthy and CVBD-suspect dogs in Portugal – a national serological study. Parasit Vector 2012, 5:62. BioMed Central Full Text
• [11]Hamer SA, Tsao JI, Walker ED, Mansfield LS, Foster ES, Hickling GJ: Use of tick surveys and serosurveys to evaluate pet dogs as a sentinel species for emerging Lyme disease. Am J Vet Res 2009, 70:49-56.
• [12]Smith FD, Ballantyne R, Morgan ER, Wall R: Estimating Lyme disease risk using pet dogs as sentinels. Comp Immunol Microbiol Infect Dis 2012, 35:163-167.
• [13]Mead P, Goel R, Kugeler K: Canine serology as adjunct to human Lyme disease surveillance. Emerg Infect Dis 2011, 17:1710-1712.
• [14]Beall MJ, Alleman AR, Breitschwerdt EB, Cohn LA, Couto CG, Dryden MW, Guptill LC, Iazbik C, Kania SA, Lathan P, Little SE, Roy A, Sayler KA, Stillman BA, Welles EG, Wolfson W, Yabsley MJ: Seroprevalence of Ehrlichia canis, Ehrlichia chaffeensis and Ehrlichia ewingii in dogs in North America. Parasit Vectors 2012, 5:29. BioMed Central Full Text
• [15]Chandrashekar R, Mainville CA, Beall MJ, O’Connor T, Eberts MD, Alleman AR, Gaunt SD, Breitschwerdt EB: Performance of a commercially available in-clinic ELISA for the detection of antibodies against Anaplasma phagocytophilum, Ehrlichia canis, and Borrelia burgdorferi and Dirofilaria immitis antigen in dogs. Am J Vet Res 2010, 71:1443-1450.
• [16]Stillman BA, Monn M, Liu J, Thatcher B, Foster P, Andrews B, Little S, Eberts M, Breitschwerdt E, Beall M, Chandrashekar R: Performance of a new commercially available in-clinic ELISA for the detection of antibodies to Ehrlichia ewingii (granulocytic ehrlichiosis) and Anaplasma platys (thrombocytopenic anaplasmosis) in dogs. JAVMA 2014. in press
• [17]Blagburn BL, Lindsay DS, Vaughn JK, Rippey NS, Wright JC, Lynn RC, Kelch WJ, Ritchie GC, Hepler DI: Prevalence of canine parasites based on fecal flotation. Comp Cont Ed Pract Vet 1996, 18:483-509.
• [18]Centers for Disease Control and Prevention (CDC)http://www.cdc.gov/mmwr/mmwr_nd/ webcite Accessed November 1, 2013
• [19]United States Census Bureau 2013. http://www.census.gov/popest/data/intercensal/index.html webcite
• [20]Kilpatrick AM, Randolph SE: Drivers, dynamics, and control of emerging vector-borne zoonotic diseases. Lancet 2012, 380:1946-1955.
• [21]Little SE: Future challenges for parasitology: vector control and one health in the Americas. Vet Parasitol 2013, 195:249-255.
• [22]Mencke N: Future challenges for parasitology: vector control and ‘One health’ in Europe: the veterinary medicinal view on CVBDs such as tick borreliosis, rickettsiosis and canine leishmaniosis. Vet Parasitol 2013, 195:256-271.
• [23]American Veterinary Medical Association (AVMA): U. S. pet ownership and demographics sourcebook, 2012. http://www.avma.org webcite
• [24]Duffy DC, Clark DD, Campbell SR, Gurney S, Perello R, Simon N: Landscape patterns of abundance of Ixodes scapularis (Acari: Ixodidae) on Shelter Island, New York. J Med Entomol 1994, 31:875-879.
• [25]Standaert SM, Dawson JE, Schaffner W, Childs JE, Biggie KL, Singleton J Jr, Gerhardt RR, Knight ML, Hutcheson RH: Ehrlichiosis in a golf-oriented retirement community. N Engl J Med 1995, 333:420-425.
• [26]Jobe DA, Nelson JA, Adam MD, Martin SA Jr: Lyme disease in urban areas, Chicago. Emerg Infect Dis 2007, 13:1799-1800.
• [27]Hamer SA, Goldberg TL, Kitron UD, Brawn JD, Anderson TK, Loss SR, Walker ED, Hamer GL: Wild birds and urban ecology of ticks and tick-borne pathogens, Chicago, Illinois, USA, 2005–2010. Emerg Infect Dis 2012, 18:1589-1595.
• [28]Snyder DE, Wiseman S, Cruthers LR, Slone RL: Ivermectin and milbemycin oxime in experimental adult heartworm (Dirofilaria immitis) infection of dogs. JVIM 2011, 25:61-64.
• [29]Blagburn BL, Dillon AR, Arther RG, Butler JM, Newton JC: Comparative efficacy of four commercially available heartworm preventive products against the MP3 laboratory strain of Dirofilaria immitis. Vet Parasitol 2011, 176:189-194.
• [30]Bowman DD: Heartworms, macrocyclic lactones, and the specter of resistance to prevention in the United States. Parasit Vectors 2012, 5:138. BioMed Central Full Text
• [31]Millen K, Kugeler KJ, Hinckley AF, Lawaczeck EW, Mead PS: Elevated Lyme disease seroprevalence among dogs in a nonendemic county: harbinger or artifact? Vector Borne Zoonotic Dis 2013, 13:340-341.
• [32]Walters LL, Lavoipierre MM: Landscape epidemiology of mosquito-borne canine heartworm (Dirofilaria immitis) in northern California, USA. I. Community-based surveys of domestic dogs in three landscapes. J Med Entomol 1984, 21:1-16.
• [33]Sacks BN, Caswell-Chen EP: Reconstructing the spread of Dirofilaria immitis in California coyotes. J Parasitol 2003, 89:319-323.
• [34]Bacon RM, Kugeler KJ, Mead PS: Surveillance for Lyme disease–United States, 1992–2006. MMWR Surveill Summ 2008, 57:1-9.
• [35]Dahlgren FS, Mandel EJ, Krebs JW, Massung RF, McQuiston JH: Increasing incidence of Ehrlichia chaffeensis and Anaplasma phagocytophilum in the United States, 2000–2007. Am J Trop Med Hyg 2011, 85:124-131.
• [36]Diuk-Wasser MA, Hoen AG, Cislo P, Brinkerhoff R, Hamer SA, Rowland M, Cortinas R, Vourc’h G, Melton F, Hickling GJ, Tsao JI, Bunikis J, Barbour AG, Kitron U, Piesman J, Fish D: Human risk of infection with Borrelia burgdorferi, the Lyme disease agent, in eastern United States. Am J Trop Med Hyg 2012, 86:320-327.
• [37]O’Connor TP, Saucier JM, Daniluk D, Stillman BA, Krah R, Rikihisa Y, Xiong Q, Yabsley MJ, Adams DS, Diniz PP, Breitschwerdt EB, Gaunt SD, Chandrashekar R: Evaluation of peptide- and recombinant protein-based assays for detection of anti-Ehrlichia ewingii antibodies in experimentally and naturally infected dogs. Am J Vet Res 2010, 71:1195-1200.
• [38]Childs JE, Paddock CD: The ascendancy of Amblyomma americanum as a vector of pathogens affecting humans in the United States. Annu Rev Entomol 2003, 48:307-337.
• [39]Nicholson WL, Paddock CD, Demma L, Traeger M, Johnson B, Dickson J, McQuiston J, Swerdlow D: Rocky Mountain spotted fever in Arizona: documentation of heavy environmental infestations of Rhipicephalus sanguineus at an endemic site. Ann N Y Acad Sci 2006, 1078:338-341.
• [40]Beeler E, Abramowicz KF, Zambrano ML, Sturgeon MM, Khalaf N, Hu R, Dasch GA, Eremeeva ME: A focus of dogs and Rickettsia massiliae-infected Rhipicephalus sanguineus in California. Am J Trop Med Hyg 2011, 84:244-249.
• [41]Cortinas R, Spomer S: Lone star tick (Acari: Ixodidae) occurrence in Nebraska: historical and current perspectives. J Med Entomol 2013, 50:244-251.
• [42]Pritt BS, Sloan LM, Johnson DK, Munderloh UG, Paskewitz SM, McElroy KM, McFadden JD, Binnicker MJ, Neitzel DF, Liu G, Nicholson WL, Nelson CM, Franson JJ, Martin SA, Cunningham SA, Steward CR, Bogumill K, Bjorgaard ME, Davis JP, McQuiston JH, Warshauer DM, Wilhelm MP, Patel R, Trivedi VA, Eremeeva ME: Emergence of a new pathogenic Ehrlichia species, Wisconsin and Minnesota, 2009. NEJM 2011, 365:422-429.
• [43]Hegarty BC, Maggi RG, Koskinen P, Beall MJ, Eberts M, Chandrashekar R, Breitschwerdt EB: Ehrlichia muris infection in a dog from Minnesota. JVIM 2012, 26:1217-1220.
• [44]Centers for Disease Control and Prevention (CDC): Anaplasmosis and ehrlichiosis - Maine, 2008. MMWR Morb Mortal Wkly Rep 2009, 58:1033-1036.
• [45]Little SE, O’Connor TP, Hempstead JE, Saucier J, Reichard MV, Meinkoth K, Meinkoth JH, Andrews B, Ullom S, Ewing SA, Chandrashekar R: Ehrlichia ewingii infection and exposure rates in dogs from the southcentral United States. Vet Parasitol 2010, 172:355-360.
• [46]Dantas-Torres F: The brown dog tick, Rhipicephalus sanguineus (Latreille, 1806) (Acari: Ixodidae): from taxonomy to control. Vet Parasitol 2008, 152:173-185.
• [47]O’Connor TP, Esty KJ, Machenry P, Hanscom JL, Bartol BA, Lawton T: Performance evaluation of Ehrlichia canis and Borrelia burgdorferi peptides in a new Dirofilaria immitis combination assay. American Heartworm Society Triannual Symposium 2002, 77-84.
• [48]O’Connor TP, Esty KJ, Hanscom JL, Shields P, Philipp MT: Dogs vaccinated with common Lyme disease vaccines do not respond to IR6, the conserved immunodominant region of the VlsE surface protein of Borrelia burgdorferi. Clin Diagn Lab Immunol 2004, 11:458-462.
• [49]Little SE: Ehrlichiosis and anaplasmosis in dogs and cats. Vet Clin North Am Small Anim Pract 2010, 40:1121-1140.
• [50]Walls JJ, Aguero-Rosenfeld M, Bakken JS, Goodman JL, Hossain D, Johnson RC, Dumler JS: Inter- and intralaboratory comparison of Ehrlichia equi and human granulocytic ehrlichiosis (HGE) agent strains for serodiagnosis of HGE by the immunofluorescent-antibody test. J Clin Microbiol 1999, 37:2968-2973.
• [51]Dumler JS, Madigan JE, Pusterla N, Bakken JS: Ehrlichioses in humans: epidemiology, clinical presentation, diagnosis, and treatment. Clin Infect Dis 2007, Suppl 1:S45-S51.
• [52]Miro G, Montyoa A, Roura X, Glavez R, Sainz A: Seropositivity rates for agents of canine vector-borne diseases in Spain: a multicenter study. Parasit Vectors 2013, 6:117. BioMed Central Full Text