Nationwide Seroprevalence of Dirofilaria immitis Antigen and Antibodies to Borrelia burgdorferi, Anaplasma spp., and Ehrlichia spp. in Shelter Cats in the United States, 2007–2011
Abstract
:1. Introduction
2. Results
2.1. B. burgdorferi
2.2. Anaplasma spp.
2.3. Ehrlichia spp.
2.4. Dirofilaria immitis
2.5. Ectoparasites
3. Discussion
4. Materials and Methods
4.1. Sample Collection and Processing
4.2. Serological Assay
4.3. Data and Statistical Analysis
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Eisen, R.J.; Kugeler, K.J.; Eisen, L.; Beard, C.B.; Paddock, C.D. Tick-Borne Zoonoses in the United States: Persistent and Emerging Threats to Human Health. ILAR J. 2017, 58, 319–335. [Google Scholar] [CrossRef] [PubMed]
- CDC. Annual Statistics from the National Notifiable Diseases Surveillance System (NNDSS). [WWW Document]. Wonder. 2021. Available online: https://wonder.cdc.gov/nndss/nndss_annual_tables_menu.asp (accessed on 7 February 2024).
- Day, M.J. One health: The importance of companion animal vector-borne diseases. Parasites Vectors 2011, 4, 49. [Google Scholar] [CrossRef] [PubMed]
- Beall, M.J.; Alleman Ar Breitschwerdt, E.B.; Cohn, L.A.; Couto, C.G.; Dryden, M.W.; Guptill, L.C.; Iazbik, C.; Kania, S.A.; Lathan, P.; Little, S.E.; et al. Seroprevalence of Ehrlichia canis, Ehrlichia chaffeensis and Ehrlichia ewingii in dogs in North America. Parasites Vectors 2012, 5, 29. [Google Scholar] [CrossRef] [PubMed]
- Mead, P.; Goel, R.; Kugeler, K. Canine Serology as Adjunct to Human Lyme Disease Surveillance. Emerg. Infect. Dis. 2011, 17, 1710–1712. [Google Scholar] [CrossRef]
- Bowman, D.; Little, S.E.; Lorentzen, L.; Shields, J.; Sullivan, M.P.; Carlin, E.P. 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. [Google Scholar] [CrossRef]
- Little, S.E.; Beall, M.J.; Bowman, D.D.; Chandrashekar, R.; Stamaris, J. Canine infection with Dirofilaria immitis, Borrelia burgdorferi, Anaplasma spp., and Ehrlichia spp. in the United States, 2010–2012. Parasites Vectors 2014, 7, 257. [Google Scholar] [CrossRef]
- Little, S.; Braff, J.; Place, J.; Buch, J.; Dewage, B.G.; Knupp, A.; Beall, M. Canine infection with Dirofilaria immitis, Borrelia burgdorferi, Anaplasma spp., and Ehrlichia spp. in the United States, 2013–2019. Parasites Vectors 2021, 14, 10. [Google Scholar] [CrossRef]
- CAPC. Parasite Prevalence Maps [WWW Document]. Companion Animal Parasite Council. 2024. Available online: https://capcvet.org/maps/ (accessed on 7 August 2024).
- Magnarelli, L.A.; Anderson, J.F.; Levine, H.R.; Levy, S.A. Tick parasitism and antibodies to Borrelia burgdorferi in cats. J. Am. Vet. Med. Assoc. 1990, 197, 63–66. [Google Scholar] [CrossRef]
- Magnarelli, L.A.; Bushmich, S.L.; IJdo, J.W.; Fikrig, E. Seroprevalence of antibodies against Borrelia burgdorferi and Anaplasma phagocytophilum in cats. Am. J. Vet. Res. 2005, 66, 1895–1899. [Google Scholar] [CrossRef]
- Hegarty, B.C.; Qurollo, B.A.; Thomas, B.; Park, K.; Chandrashekar, R.; Beall, M.J.; Thatcher, B.; Breitschwerdt, E.B. Serological and molecular analysis of feline vector-borne anaplasmosis and ehrlichiosis using species-specific peptides and PCR. Parasites Vectors 2015, 8, 320. [Google Scholar] [CrossRef]
- Shannon, A.B.; Rucinsky, R.; Gaff, H.D.; Brinkerhoff, R.J. Borrelia miyamotoi, other vector-borne agents in cat blood and ticks in eastern Maryland. EcoHealth 2017, 14, 816–820. [Google Scholar] [CrossRef] [PubMed]
- Hoyt, K.; Chandrashekar, R.; Beall, M.; Leutenegger, C.; Lappin, M.R. Evidence for clinical anaplasmosis and borreliosis in cats in Maine. Top. Companion Anim. Med. 2018, 33, 40–44. [Google Scholar] [CrossRef] [PubMed]
- Galemore, E.R.; Labato, M.A.; O’Neil, E. Prevalence of Anaplasma phagocytophilum infection in feral cats in Massachusetts. JFMS Open Rep. 2018, 4, 2055116917753804. [Google Scholar] [CrossRef]
- Luria, B.J.; Levy, J.K.; Lappin, M.R.; Breitschwerdt, E.B.; Legendre, A.M.; Hernandez, J.A.; Gorman, S.P.; Lee, I.T. Prevalence of infectious diseases in feral cats in northern Florida. J. Feline Med. Surg. 2004, 6, 287–296. [Google Scholar] [CrossRef]
- Lappin, M.R.; Griffin, B.; Brunt, J.; Riley, A.; Burney, D.; Hawley, J.; Brewer, M.M.; Jensen, W.A. Prevalence of Bartonella species, Haemoplasma species, Ehrlichia species, Anaplasma phagocytophilum, and Neorickettsia risticii DNA in the blood of cats and their fleas in the United States. J. Feline Med. Surg. 2006, 8, 85–90. [Google Scholar] [CrossRef]
- Hackett, T.B.; Jensen, W.A.; Lehman, T.L.; Hohenhaus, A.E.; Crawford, P.C.; Giger, U.; Lappin, M.R. Prevalence of DNA of Mycoplasma haemofelis, ‘Candidatus Mycoplasma haemominutum’, Anaplasma phagocytophilum, and species of Bartonella, Neorickettsia, and Ehrlichia in cats used as blood donors in the United States. J. Am. Vet. Med. Assoc. 2006, 229, 700–705. [Google Scholar] [CrossRef]
- Ishak, A.M.; Radecki, S.; Lappin, M.R. Prevalence of Mycoplasma haemofelis, “Candidatus Mycoplasma haemominutum”, Bartonella species, Ehrlichia species, and Anaplasma phagocytophilum DNA in the blood of cats with anemia. J. Feline Med. Surg. 2007, 9, 1–7. [Google Scholar] [CrossRef]
- Billeter, S.A.; Spencer, J.A.; Griffin, B.; Dykstra, C.C.; Blagburn, B.L. Prevalence of Anaplasma phagocytophilum in domestic felines in the United States. Vet. Parasitol. 2007, 147, 194–198. [Google Scholar] [CrossRef]
- Scorza, A.V.; Lappin, M.R. Prevalence of selected zoonotic and vector-borne agents in dogs and cats on the Pine Ridge Reservation. Vet. Sci. 2017, 4, 43. [Google Scholar] [CrossRef]
- Levy, J.K.; Lappin, M.R.; Glaser, A.L.; Birkenheuer, A.J.; Anderson, T.C.; Edinboro, C.H. Prevalence of infectious diseases in cats and dogs rescued following Hurricane Katrina. J. Am. Vet. Med. Assoc. 2011, 238, 311–317. [Google Scholar] [CrossRef]
- Beall, M.J.; Mainville, C.A.; Arguello-Marin, A.; Clark, G.; Lemieux, C.; Saucier, J.; Thatcher, B.; Breitschwerdt, E.B.; Cohn, L.A.; Qurollo, B.A.; et al. An Improved Point-of-Care ELISA for the Diagnosis of Anaplasmosis and Ehrlichiosis During the Acute Phase of Tick-Borne Infections in Dogs. Top. Companion Anim. Med. 2022, 51, 100735. [Google Scholar] [CrossRef]
- Goldstein, R.E.; Eberts, M.D.; Beall, M.J.; Thatcher, B.; Chandrashekar, R.; Alleman, A.R. Performance comparison of SNAP® 4Dx® Plus and AccuPlex®4 for the detection of antibodies to Borrelia burgdorferi and Anaplasma phagocytophilum. Int. J. Appl. Res. Vet. Med. 2014, 12, 141–147. [Google Scholar]
- Krcatovich, E.H.; Workman, J.; Stasiak, K.; Goldstein, R.E. Comparative evaluation of Borrelia burgdorferi antibody detection between the VetScan Flex4 and SNAP 4Dx Plus. Top. Companion Anim. Med. 2024, 59, 100862. [Google Scholar] [CrossRef] [PubMed]
- Lappin, M.R.; Chandrashekar, R.; Stillman, B.; Liu, J.; Mather, T.N. Evidence of Anaplasma phagocytophilum and Borrelia burgdorferi infection in cats after exposure to wild-caught adult Ixodes scapularis. J. VET Diagn. Investig. 2015, 27, 522–525. [Google Scholar] [CrossRef] [PubMed]
- Lappin, M.R.; Little, S.E. Unpublished Study Data. 2010. [Google Scholar]
- Dillon, R. Feline heartworm disease. In Proceedings of the Heartworm Symposium ’86: Trienniel American Heartworm Society Symposium, New Orleans, LA, USA, 21–23 March 1986; pp. 149–154. [Google Scholar]
- Hays, K.M.; Rodriguez, J.Y.; Little, S.E.; Litster, A.L.; Mwacalimba, K.K.; Sundstrom, K.D.; Amodie, D.M.; Serrano, M.A.; Guerios, S.D.; Lane, J.N.; et al. Heartworm prevalence in dogs versus cats: Multiple diagnostic modalities provide new insights. Vet. Parasitol. 2020, 277, 100027. [Google Scholar] [CrossRef]
- American Heartworm Society. Available online: https://www.heartwormsociety.org/veterinary-resources/american-heartworm-society-guidelines (accessed on 15 July 2024).
- Smith, R.C.; Barrantes Murillo, D.F.; Starkey, L.A.; The Prevalence and Diagnosis of Feline Heartworm Infection. Today’s Veterinary Practice. 2024. Available online: https://todaysveterinarypractice.com/parasitology/the-prevalence-and-diagnosis-of-feline-heartworm-infection/ (accessed on 12 September 2024).
- Baker, A.; Wang, H.-H.; Mogg, M.; Derouen, Z.; Borski, J.; Grant, W.E. Increasing incidence of anaplasmosis in the United States, 2012 through 2016. Vector-Borne Zoonotic Dis. 2020, 20, 855–859. [Google Scholar] [CrossRef]
- Schwartz, A.M. Surveillance for Lyme disease—United States, 2008–2015. MMWR Surveill Summ 2017, 66, 1–12. [Google Scholar] [CrossRef]
- Thomas, J.E.; Staubus, L.; Goolsby, J.L.; Reichard, M.V. Ectoparasites of free-roaming domestic cats in the central United States. Vet. Parasitol. 2016, 228, 17–22. [Google Scholar] [CrossRef]
- Saleh, M.N.; Sundstrom, K.D.; Duncan, K.T.; Ientile, M.M.; Jordy, J.; Ghosh, P.; Little, S.E. Show us your ticks: A survey of ticks infesting dogs and cats across the USA. Parasites Vectors 2019, 12, 595. [Google Scholar] [CrossRef]
- Levy, J.K.; Burling, A.N.; Crandall, M.M.; Tucker, S.J.; Wood, E.G.; Foster, J.D. Seroprevalence of heartworm infection, risk factors for seropositivity, and frequency of prescribing heartworm preventives for cats in the United States and Canada. J. Am. Vet. Med. Assoc. 2017, 250, 873–880. [Google Scholar] [CrossRef]
- Murillo, D.F.B.; Starkey, L.; Wood, T.; Smith, R.; Blagburn, B.; Bowles, J.; Allen, H.; Lewis, C.; Shu, Y.; Wang, C. A nationwide serological survey for Dirofilaria immitis in companion cats in the United States of America: 3.5% antibody and 0.3% antigen positivity. Parasites Vectors 2023, 16, 296. [Google Scholar] [CrossRef] [PubMed]
- Drake, J.; Parrish, R.S. Dog importation and changes in heartworm prevalence in Colorado 2013–2017. Parasites Vectors 2019, 12, 207. [Google Scholar] [CrossRef] [PubMed]
- Agriculture Department; Strickland, R.K. Ticks of Veterinary Importance, Agricultural Handbook No. 485; Government, Agriculture Department: Washington, DC, USA, 1975.
- Sanford, L.G.; Hays, K.L.; Kirby, L. Fleas (Siphonaptera) of Alabama and Their Host Relationships; Agricultural Experiment Station, Auburn Univerisyt: Auburn, AL, USA, 1974. [Google Scholar]
- Chandrashekar, R.; Mainville, C.A.; Beall, M.J.; O’Connor, T.; Eberts, M.D.; Alleman, A.R.; Gaunt, S.D.; Breitschwerdt, E.B. 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. [Google Scholar] [CrossRef] [PubMed]
- Stillman, B.A.; Monn, M.; Liu, J.; Thatcher, B.; Foster, P.; Andrews, B.; Little, S.; Eberts, M.; Breitschwerdt, E.B.; Beall, M.J.; et al. Performance of a commercially available in-clinic ELISA for detection of antibodies against Anaplasma phagocytophilum, Anaplasma platys, Borrelia burgdorferi, Ehrlichia canis, and Ehrlichia ewingii and Dirofilaria immitis antigen in dogs. J. Am. Vet. Med. Assoc. 2014, 245, 80–86. [Google Scholar] [CrossRef]
- O’Connor, T.P.; Hanscom, J.L.; Hegarty, B.C.; Groat, R.G.; Breitschwerdt, E.B. Comparison of an indirect immunofluorescence assay, western blot analysis, and a commercially available ELISA for detection of Ehrlichia canis antibodies in canine sera. Am. J. Veter-Res. 2006, 67, 206–210. [Google Scholar] [CrossRef]
- Schvartz, G.; Epp, T.; Burgess, H.J.; Chilton, N.B.; Pearl, D.L.; Lohmann, K.L. Seroprevalence of equine granulocytic anaplasmosis and lyme borreliosis in Canada as determined by a point-of-care enzyme-linked immunosorbent assay (ELISA). Can. Vet. J. 2015, 56, 575–580. [Google Scholar]
- Veronesi, F.; Passamonti, F.; Moretti, A.; Morganti, G.; Vardi, D.M.; Laus, F.; Marenzoni, M.L.; Spaterna, A.; Coletti, M.; Piergili Fioretti, D. Evaluation of the performance of a rapid enzyme-linked immunosorbent assay in the detection of Anaplasma phagocytophilum antibodies in horses. Vector-Borne Zoonotic Dis. 2014, 14, 317–323. [Google Scholar] [CrossRef]
- Blagburn, B.L.; Lindsay, D.; Vaughan, J.L.; Rippey, N.S.; Wright, J.; Lynn, R.C.; Kelch, W.J.; Ritchie, G.C.; Hepler, D.I. Prevalence of canine parasites based on fecal flotation. Compend. Contin. Educ. Pract. Vet. 1996, 18, 483–509. [Google Scholar]
Geographic Distribution | Sample Source | Detection Method | Prevalence | Reference |
---|---|---|---|---|
B. burgdorferi | ||||
Northeast | Owned pet cats | Ab detection | 14.1% (10/71) | [10] |
Northeast | Owned pet cats | Ab detection | 47.31% (44/93) | [11] |
Nationwide | Submitted for Dx at NCSU-VBDDL | Ab detection | 5.45% (39/715) | [12] |
MD | Owned pet cats | Ab detection PCR | 28.00% (7/25) 0.00% (0/49) | [13] |
ME | Owned pet cats | Ab detection | 18.23% (29/159) | [14] |
MA | Feral cats | Ab detection | 24.00% (42/175) | [15] |
Anaplasma spp. | ||||
FL | Free roaming cats | PCR | 0.00% (0/484) | [16] |
Northeast | Owned pet cats | Ab detection (IFA and ELISA) | 37.63% (35/93) 30.11% (28/93) | [11] |
AL, MD, TX | Owned pet and sheltered cats | PCR | 0.00% (0/92) | [17] |
IL, OK, CO, MD OR, NY | Blood donor cats | PCR | 0.00% (0/146) | [18] |
Unreported | Anemic and healthy owned cats | PCR | 0.00% (0/176) | [19] |
AL, FL, CA WI, MI, RI | Owned pet and sheltered cats | Ab detection | 4.30% (20/460) | [20] |
Nationwide | Submitted for Dx at NCSU-VBDDL | Ab detection and PCR | Anapl genus Ab 0.70% (5/715) A. phag Ab 1.80% (13/715) A. platys Ab 0.00% (0/715) A. phag PCR 0.68% (5/737) A. platys PCR 0.41% (3/737) | [12] |
MD | Owned pet cats | Ab detection | 4.00% (1/25) | [13] |
SD | Owned pet cats | PCR | 0.00% (0/39) | [21] |
MA | Feral cats | Ab detection PCR | 9.71% (17/175) 6.94% (12/173) | [15] |
Ehrlichia spp. | ||||
FL | Free roaming cats | PCR | 0.00% (0/484) | [16] |
IL, OK, CO, MD OR, NY | Blood donor cats | PCR | 0.00% (0/146) | [18] |
AL, MD, TX | Owned pet and sheltered cats | PCR | 0.00% (0/92) | [17] |
Unreported | Anemic and healthy owned cats | PCR | 0.00% (0/176) | [19] |
Gulf Coast Region | Unknown history following natural disaster | PCR | 0.00% (0/47) | [22] |
Nationwide | Submitted for Dx at NCSU-VBDDL | Ab detection PCR | Ehrl genus Ab 0.70% (5/715) E. canis Ab 0.70% (5/715) E. ewingii Ab 0.14% (1/715) E. chaffeensis Ab 0.28% (2/715) E. canis PCR 0.14% (1/737) E. ewingii PCR 0.41% (3/737) E. chaffeensis PCR 0.27% (2/737) | [12] |
MD | Owned pet cats | Ab detection | 12.00% (3/25) | [13] |
SD | Owned pet cats | PCR | 0.00% (0/39) | [21] |
B. burgdorferi | Anaplasma spp. | Ehrlichia spp. | D. immitis | |
---|---|---|---|---|
Total | 1.88% (42/2232) | 0.54% (12/2232) | 0.09% (2/2232) | 0.55% (8/1457) |
Northeast | 5.34% (34/637) | 1.10% (7/637) | 0.31% (2/637) | 1.29% (5/389) |
Midwest | 0.66% (5/756) | 0.53% (4/756) | 0.00% (0/756) | 0.00% (0/518) |
South | 0.56% (2/355) | 0.00% (0/355) | 0.00% (0/355) | 0.64% (2/312) |
West | 0.21% (1/484) | 0.21% (1/484) | 0.00% (0/484) | 0.42% (1/238) |
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2024 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Smith, R.C.; Starkey, L.A.; Bowles, J.V.; Butler, J.M.; Mount, J.; Land, T.M.; Blagburn, B.L. Nationwide Seroprevalence of Dirofilaria immitis Antigen and Antibodies to Borrelia burgdorferi, Anaplasma spp., and Ehrlichia spp. in Shelter Cats in the United States, 2007–2011. Parasitologia 2024, 4, 332-344. https://doi.org/10.3390/parasitologia4040029
Smith RC, Starkey LA, Bowles JV, Butler JM, Mount J, Land TM, Blagburn BL. Nationwide Seroprevalence of Dirofilaria immitis Antigen and Antibodies to Borrelia burgdorferi, Anaplasma spp., and Ehrlichia spp. in Shelter Cats in the United States, 2007–2011. Parasitologia. 2024; 4(4):332-344. https://doi.org/10.3390/parasitologia4040029
Chicago/Turabian StyleSmith, Rachel C., Lindsay A. Starkey, Joy V. Bowles, Jamie M. Butler, Jane Mount, Tracy M. Land, and Byron L. Blagburn. 2024. "Nationwide Seroprevalence of Dirofilaria immitis Antigen and Antibodies to Borrelia burgdorferi, Anaplasma spp., and Ehrlichia spp. in Shelter Cats in the United States, 2007–2011" Parasitologia 4, no. 4: 332-344. https://doi.org/10.3390/parasitologia4040029
APA StyleSmith, R. C., Starkey, L. A., Bowles, J. V., Butler, J. M., Mount, J., Land, T. M., & Blagburn, B. L. (2024). Nationwide Seroprevalence of Dirofilaria immitis Antigen and Antibodies to Borrelia burgdorferi, Anaplasma spp., and Ehrlichia spp. in Shelter Cats in the United States, 2007–2011. Parasitologia, 4(4), 332-344. https://doi.org/10.3390/parasitologia4040029