Skip directly to site content Skip directly to page options Skip directly to A-Z link Skip directly to A-Z link Skip directly to A-Z link
Volume 30, Number 12—December 2024
Online Report

Operational Risk Assessment Tool for Evaluating Leishmania infantum Introduction and Establishment in the United States through Dog Importation1

David R. Marquez2Comments to Author , Anne Straily2, Keeve Nachman, Douglas E. Norris, Meghan F. Davis3, and Christine A. Petersen3
Author affiliation: US Army Veterinary Services, Aberdeen Proving Ground, Maryland, USA (D.R. Marquez); Johns Hopkins University, Baltimore, Maryland, USA (D.R. Marquez, K. Nachman, D.E. Norris, M.F. Davis); Centers for Disease Control and Prevention, Atlanta, Georgia, USA (A. Straily); University of Iowa, Iowa City, Iowa, USA (C.A. Petersen)

Main Article

Figure 8

Combined probability matrix for entry and exposure assessments developed from an operational risk assessment tool for evaluating Leishmania infantum introduction and establishment in the United States through dog importation. Modified from Wieland et al. (17).

Figure 8. Combined probability matrix for entry and exposure assessments developed from an operational risk assessment tool for evaluating Leishmania infantum introduction and establishment in the United States through dog importation. Modified from Wieland et al. (17).

Main Article

References
  1. Wright  I, Jongejan  F, Marcondes  M, Peregrine  A, Baneth  G, Bourdeau  P, et al. Parasites and vector-borne diseases disseminated by rehomed dogs. Parasit Vectors. 2020;13:546. DOIPubMedGoogle Scholar
  2. McQuiston  JH, Wilson  T, Harris  S, Bacon  RM, Shapiro  S, Trevino  I, et al. Importation of dogs into the United States: risks from rabies and other zoonotic diseases. Zoonoses Public Health. 2008;55:421–6. DOIPubMedGoogle Scholar
  3. Wright  I, Whitfield  V, Hanaghan  R, Upjohn  M, Boyden  P. Analysis of exotic pathogens found in a large group of imported dogs following an animal welfare investigation. Vet Rec. 2023;193:e2996. DOIPubMedGoogle Scholar
  4. Centers for Disease Control and Prevention. Guidance regarding agency interpretation of “rabies-free” as it relates to the importation of dogs into the United States. Federal Register. 2019 Jan 31 [cited 2023 May 22]. https://www.federalregister.gov/d/2019-00506
  5. United States Department of Agriculture. Report on the importation of live dogs into the United States. 2019 Jun 25 [cited 2023 May 22]. http://www.naiaonline.org/uploads/WhitePapers/USDA_DogImportReport6-25-2019.pdf
  6. Herricks  JR, Hotez  PJ, Wanga  V, Coffeng  LE, Haagsma  JA, Basáñez  MG, et al. The global burden of disease study 2013: What does it mean for the NTDs? PLoS Negl Trop Dis. 2017;11:e0005424. DOIPubMedGoogle Scholar
  7. Vilas-Boas  DF, Nakasone  EKN, Gonçalves  AAM, Lair  DF, Oliveira  DS, Pereira  DFS, et al. Global distribution of canine visceral leishmaniasis and the role of the dog in the epidemiology of the disease. Pathogens. 2024;13:455. DOIPubMedGoogle Scholar
  8. Burza  S, Croft  SL, Boelaert  M. Leishmaniasis. Lancet. 2018;392:951–70. DOIPubMedGoogle Scholar
  9. Duprey  ZH, Steurer  FJ, Rooney  JA, Kirchhoff  LV, Jackson  JE, Rowton  ED, et al. Canine visceral leishmaniasis, United States and Canada, 2000-2003. Emerg Infect Dis. 2006;12:440–6. DOIPubMedGoogle Scholar
  10. Toepp  AJ, Schaut  RG, Scott  BD, Mathur  D, Berens  AJ, Petersen  CA. Leishmania incidence and prevalence in U.S. hunting hounds maintained via vertical transmission. Vet Parasitol Reg Stud Reports. 2017;10:75–81. DOIPubMedGoogle Scholar
  11. Bruhn  FRP, Morais  MHF, Cardoso  DL, Bruhn  NCP, Ferreira  F, Rocha  CMBMD. Spatial and temporal relationships between human and canine visceral leishmaniases in Belo Horizonte, Minas Gerais, 2006-2013. Parasit Vectors. 2018;11:372. DOIPubMedGoogle Scholar
  12. World Health Organization. Leishmaniasis. 2023 Jan 12 [cited 2023 May 22]. https://www.who.int/en/news-room/fact-sheets/detail/leishmaniasis
  13. Martín-Sánchez  J, Morales-Yuste  M, Acedo-Sánchez  C, Barón  S, Díaz  V, Morillas-Márquez  F. Canine leishmaniasis in southeastern Spain. Emerg Infect Dis. 2009;15:795–8. DOIPubMedGoogle Scholar
  14. Gin  TE, Lashnits  E, Wilson  JM, Breitschwerdt  EB, Qurollo  B. Demographics and travel history of imported and autochthonous cases of leishmaniosis in dogs in the United States and Canada, 2006 to 2019. J Vet Intern Med. 2021;35:954–64. DOIPubMedGoogle Scholar
  15. Curtin  JM, Aronson  NE. Leishmaniasis in the United States: emerging issues in a region of low endemicity. Microorganisms. 2021;9:578. DOIPubMedGoogle Scholar
  16. European Centre for Disease Prevention and Control. Operational tool on rapid risk assessment methodology. 2019 Mar 14 [cited 2023 May 22] https://www.ecdc.europa.eu/sites/default/files/documents/operational-tool-rapid-risk-assessment-methodolgy-ecdc-2019.pdf
  17. Wieland  B, Dhollander  S, Salman  M, Koenen  F. Qualitative risk assessment in a data-scarce environment: a model to assess the impact of control measures on spread of African Swine Fever. Prev Vet Med. 2011;99:4–14. DOIPubMedGoogle Scholar
  18. World Health Organization, Food and Agriculture Organization of the United Nations, and World Organisation for Animal Health. Joint risk assessment operational tool (JRA OT): an operational tool of the tripartite zoonoses guide. 2021 Mar 9 [cited 2023 May 22]. https://www.who.int/publications/i/item/9789240015142
  19. World Organisation for Animal Health. Handbook on import risk analysis for animals and animal products, 2nd edition. Paris: The Organisation; 2010.
  20. Food and Agriculture Organization of the United Nations. Technical guidelines on rapid risk assessment for animal health threats. FAO animal production and health guidelines no. 24. Rome: The Organization; 2021.
  21. Department of Agriculture and Water Resources. Biosecurity import risk analysis guidelines, 2016: managing biosecurity risks for imports into Australia. Canberra: Department of Agriculture and Water Resources; 2016.
  22. McKenna  M, Attipa  C, Tasker  S, Augusto  M. Leishmaniosis in a dog with no travel history outside of the UK. Vet Rec. 2019;184:441. DOIPubMedGoogle Scholar
  23. Toepp  AJ, Bennett  C, Scott  B, Senesac  R, Oleson  JJ, Petersen  CA. Maternal Leishmania infantum infection status has significant impact on leishmaniasis in offspring. PLoS Negl Trop Dis. 2019;13:e0007058. DOIPubMedGoogle Scholar
  24. Silva  FL, Oliveira  RG, Silva  TM, Xavier  MN, Nascimento  EF, Santos  RL. Venereal transmission of canine visceral leishmaniasis. Vet Parasitol. 2009;160:55–9. DOIPubMedGoogle Scholar
  25. Schantz  PM, Steurer  FJ, Duprey  ZH, Kurpel  KP, Barr  SC, Jackson  JE, et al. Autochthonous visceral leishmaniasis in dogs in North America. J Am Vet Med Assoc. 2005;226:1316–22. DOIPubMedGoogle Scholar
  26. Naucke  TJ, Amelung  S, Lorentz  S. First report of transmission of canine leishmaniosis through bite wounds from a naturally infected dog in Germany. Parasit Vectors. 2016;9:256. DOIPubMedGoogle Scholar
  27. McGrotty  Y, Kilpatrick  S, Magowan  D, Colville  R. Canine leishmaniosis in a non-travelled dog. Vet Rec. 2023;192:174–6. DOIPubMedGoogle Scholar
  28. Morales-Yuste  M, Martín-Sánchez  J, Corpas-Lopez  V. Canine leishmaniasis: update on epidemiology, diagnosis, treatment, and prevention. Vet Sci. 2022;9:387. DOIPubMedGoogle Scholar
  29. Esch  KJ, Petersen  CA. Transmission and epidemiology of zoonotic protozoal diseases of companion animals. Clin Microbiol Rev. 2013;26:58–85. DOIPubMedGoogle Scholar
  30. Pereira  MA, Santos  R, Oliveira  R, Costa  L, Prata  A, Gonçalves  V, et al. Prognostic factors and life expectancy in canine leishmaniosis. Vet Sci. 2020;7:128. DOIPubMedGoogle Scholar
  31. Berger  BA, Bartlett  AH, Saravia  NG, Galindo Sevilla  N. Pathophysiology of leishmania infection during pregnancy. Trends Parasitol. 2017;33:935–46. DOIPubMedGoogle Scholar
  32. Pineda  JA, Martín-Sánchez  J, Macías  J, Morillas  F. Leishmania spp infection in injecting drug users. Lancet. 2002;360:950–1. DOIPubMedGoogle Scholar
  33. Miró  G, López-Vélez  R. Clinical management of canine leishmaniosis versus human leishmaniasis due to Leishmania infantum: Putting “One Health” principles into practice. Vet Parasitol. 2018;254:151–9. DOIPubMedGoogle Scholar
  34. Franssen  SU, Sanders  MJ, Berriman  M, Petersen  CA, Cotton  JA. Geographic origin and vertical transmission of Leishmania infantum parasites in hunting hounds, United States. Emerg Infect Dis. 2022;28:1211–23. DOIPubMedGoogle Scholar
  35. Schaut  RG, Robles-Murguia  M, Juelsgaard  R, Esch  KJ, Bartholomay  LC, Ramalho-Ortigao  M, et al. Vectorborne transmission of Leishmania infantum from hounds, United States. Emerg Infect Dis. 2015;21:2209–12. DOIPubMedGoogle Scholar
  36. Young  DG. Phlebotomine sand flies of North America (Diptera: Psychodidae). Mosq News. 1984;44:2.
  37. McHugh  CP, Grogl  M, Kreutzer  RD. Isolation of Leishmania mexicana (Kinetoplastida: Trypanosomatidae) from Lutzomyia anthophora (Diptera: Psychodidae) collected in Texas. J Med Entomol. 1993;30:631–3. DOIPubMedGoogle Scholar
  38. Beasley  EA, Mahachi  KG, Petersen  CA. Possibility of Leishmania transmission via Lutzomyia spp. sand flies within the USA and implications for human and canine autochthonous infection. Curr Trop Med Rep. 2022;9:160–8. DOIPubMedGoogle Scholar
  39. Lawyer  PG, Young  DG. Experimental transmission of Leishmania mexicana to hamsters by bites of phlebotomine sand flies (Diptera: Psychodidae) from the United States. J Med Entomol. 1987;24:458–62. DOIPubMedGoogle Scholar
  40. Endris  RG, Young  DG, Perkins  PV. Experimental transmission of Leishmania mexicana by a North American sand fly, Lutzomyia anthophora (Diptera: Psychodidae). J Med Entomol. 1987;24:243–7. DOIPubMedGoogle Scholar
  41. Lawyer  PG, Young  DG, Butler  JF, Akin  DE. Development of Leishmania mexicana in Lutzomyia diabolica and Lutzomyia shannoni (Diptera: Psychodidae). J Med Entomol. 1987;24:347–55. DOIPubMedGoogle Scholar
  42. Travi  BL, Ferro  C, Cadena  H, Montoya-Lerma  J, Adler  GH. Canine visceral leishmaniasis: dog infectivity to sand flies from non-endemic areas. Res Vet Sci. 2002;72:83–6. DOIPubMedGoogle Scholar
  43. Courtenay  O, Peters  NC, Rogers  ME, Bern  C. Combining epidemiology with basic biology of sand flies, parasites, and hosts to inform leishmaniasis transmission dynamics and control. PLoS Pathog. 2017;13:e1006571. DOIPubMedGoogle Scholar
  44. Scorza  BM, Mahachi  KG, Cox  AC, Toepp  AJ, Leal-Lima  A, Kumar Kushwaha  A, et al. Leishmania infantum xenodiagnosis from vertically infected dogs reveals significant skin tropism. PLoS Negl Trop Dis. 2021;15:e0009366. DOIPubMedGoogle Scholar
  45. Paltrinieri  S, Solano-Gallego  L, Fondati  A, Lubas  G, Gradoni  L, Castagnaro  M, et al.; Canine Leishmaniasis Working Group, Italian Society of Veterinarians of Companion Animals. Guidelines for diagnosis and clinical classification of leishmaniasis in dogs. J Am Vet Med Assoc. 2010;236:1184–91. DOIPubMedGoogle Scholar
  46. Miró  G, Wright  I, Michael  H, Burton  W, Hegarty  E, Rodón  J, et al. Seropositivity of main vector-borne pathogens in dogs across Europe. Parasit Vectors. 2022;15:189. DOIPubMedGoogle Scholar
  47. Martín-Sánchez  J, Rodríguez-Granger  J, Morillas-Márquez  F, Merino-Espinosa  G, Sampedro  A, Aliaga  L, et al. Leishmaniasis due to Leishmania infantum: Integration of human, animal and environmental data through a One Health approach. Transbound Emerg Dis. 2020;67:2423–34. DOIPubMedGoogle Scholar
  48. Estevam  LGTM, Veloso  LB, Silva  GG, Mori  CC, Franco  PF, Lima  ACVMR, et al. Leishmania infantum infection rate in dogs housed in open-admission shelters is higher than of domiciled dogs in an endemic area of canine visceral leishmaniasis. Epidemiological implications. Acta Trop. 2022;232:106492. DOIPubMedGoogle Scholar
  49. Hamel  D, Silaghi  C, Pfister  K. Arthropod-borne infections in travelled dogs in Europe. Parasite. 2013;20:9. DOIPubMedGoogle Scholar
  50. Teske  E, van Knapen  F, Beijer  EG, Slappendel  RJ. Risk of infection with Leishmania spp. in the canine population in the Netherlands. Acta Vet Scand. 2002;43:195–201. DOIPubMedGoogle Scholar

Main Article

1Preliminary results from this study were presented at the American Society for Tropical Medicine and Hygiene Annual Meeting; October 18–22, 2023; Chicago, Illinois, USA.

2These first authors contributed equally to this article.

3These senior authors contributed equally to this article.

Page created: October 18, 2024
Page updated: November 26, 2024
Page reviewed: November 26, 2024
The conclusions, findings, and opinions expressed by authors contributing to this journal do not necessarily reflect the official position of the U.S. Department of Health and Human Services, the Public Health Service, the Centers for Disease Control and Prevention, or the authors' affiliated institutions. Use of trade names is for identification only and does not imply endorsement by any of the groups named above.
file_external