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Volume 28, Number 6—June 2022

Geographic Origin and Vertical Transmission of Leishmania infantum Parasites in Hunting Hounds, United States

Susanne U. FranssenComments to Author , Mandy J. Sanders, Matt Berriman, Christine A. Petersen1, and James A. Cotton1
Author affiliations: Ludwig-Maximilians-Universität Munich, Munich, Germany (S.U. Franssen); Wellcome Sanger Institute, Hinxton, UK (S.U. Franssen, M.J. Sanders, M. Berriman, J.A. Cotton); University of Iowa College of Public Health, Iowa City, Iowa, USA (C.A. Petersen); Center for Emerging Infectious Diseases, University of Iowa, Iowa City (C.A. Petersen)

Main Article


Summary of groups compared in analysis of geographic origin and vertical transmission of Leishmania infantum in hunting hounds, United States*

Group name Sample size Sample names Location Isolation year Time span of isolations, y Host Disease phenotype Source
foxymo_01, foxymo_02, foxymo_03, foxymo_04, foxymo_05, foxymo_06, foxymo_07
Midwestern United States
This study
BR_d 5
BR_7VLd, BR_11VLd, BR_15VLd, BR_16VLd, BR_17VLd
Rio Grande do Norte, Brazil
NT16, TH4, TH5, TH6, LRC-L1275
BR_1VLh90, BR_2VLh90, BR_3VLh90, BR_4VLh90, BR_5VLh90
Rio Grande do Norte, Brazil
BR_12VLh, BR_14VLh, BR_19VLh, BR_8Ah, BR_9Ah, BR_18Ah
Rio Grande do Norte, Brazil
VL or asymptomatic
MA01A, MA02A, MA03A, MA04A, MA05A, MA07A
Maranhão, Brazil
MG11A, MG12A, MG13A, MG14A, MG15A, MG16A, MG17A, MG18A, MG19A
Minas Gerais, Brazil
PI01A, PI02A, PI03A, PI04A, PI05A, PI07A, PI08A, PI09A, PI10A, PI11A, PI12A
Piauí, Brazil
CH_mix 7
Human, dog, raccoon dog
VL, unknown
FR_mix 4
LEM1985, LEM3278, LPN114, RM1
Human, dog
CanL, unknown
IP_mix† 7
NT16, TH4, TH5, TH6, LRC-L1275, LRC-L1296, LRC-L1303
Israel/ Palestine
Human, dog
IT_mix 5
ISS174, ISS2420, ISS2426, ISS2429, ISS2508
Human, dog, sand fly
VL, CanL, sand fly
SP_mix‡ 5 LinJPCM5, BCN83, BCN87, IMT373cl1, IMT260 Spain/ Portugal 1987–2005 19 Human, dog CL, VL, unknown (38, 40),

*Samples and corresponding groups were chosen from the total of 99 isolates (Appendix 2 Figure 2) to represent geographic regions or countries with at least 5 samples available and a focus on groups with dog isolates only, humans only, and a mixture of hosts for comparison. †Samples in groups IS_d are also part of group IP_mix and are indicated in bold. ‡The group SP_mix contains only isolates from Spain and Portugal that are in the clade of the known including several known MON-1 samples. The isolates Inf055, Inf004 from the non–MON-1 clade are not included.

Main Article

  1. Miró  G, Petersen  C, Cardoso  L, Bourdeau  P, Baneth  G, Solano-Gallego  L, et al. Novel areas for prevention and control of canine leishmaniosis [Erratum in: Trends Parasitol. 2017;33:718–30]. Trends Parasitol. 2017;33:71830. DOIPubMedGoogle Scholar
  2. Lima  ID, Lima  ALM, Mendes-Aguiar  CO, Coutinho  JFV, Wilson  ME, Pearson  RD, et al. Changing demographics of visceral leishmaniasis in northeast Brazil: Lessons for the future. PLoS Negl Trop Dis. 2018;12:e0006164. DOIPubMedGoogle Scholar
  3. Gavgani  ASM, Mohite  H, Edrissian  GH, Mohebali  M, Davies  CR. Domestic dog ownership in Iran is a risk factor for human infection with Leishmania infantum. Am J Trop Med Hyg. 2002;67:5115. DOIPubMedGoogle Scholar
  4. Bsrat  A, Berhe  M, Gadissa  E, Taddele  H, Tekle  Y, Hagos  Y, et al. Serological investigation of visceral Leishmania infection in human and its associated risk factors in Welkait District, Western Tigray, Ethiopia. Parasite Epidemiol Control. 2018;3:1320. DOIPubMedGoogle Scholar
  5. Lima  ÁLM, de Lima  ID, Coutinho  JFV, de Sousa  ÚPST, Rodrigues  MAG, Wilson  ME, et al. Changing epidemiology of visceral leishmaniasis in northeastern Brazil: a 25-year follow-up of an urban outbreak. Trans R Soc Trop Med Hyg. 2017;111:4407. DOIPubMedGoogle Scholar
  6. Bates  PA. Transmission of Leishmania metacyclic promastigotes by phlebotomine sand flies. Int J Parasitol. 2007;37:1097106. DOIPubMedGoogle Scholar
  7. 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
  8. Grinnage-Pulley  T, Scott  B, Petersen  CA. A mother’s gift: congenital transmission of Trypanosoma and Leishmania species. PLoS Pathog. 2016;12:e1005302. DOIPubMedGoogle Scholar
  9. Boggiatto  PM, Gibson-Corley  KN, Metz  K, Gallup  JM, Hostetter  JM, Mullin  K, et al. Transplacental transmission of Leishmania infantum as a means for continued disease incidence in North America. PLoS Negl Trop Dis. 2011;5:e1019. DOIPubMedGoogle Scholar
  10. Petersen  CA. New means of canine leishmaniasis transmission in north america: the possibility of transmission to humans still unknown. Interdiscip Perspect Infect Dis. 2009;2009:802712. DOIPubMedGoogle Scholar
  11. da Silva  SM, Ribeiro  VM, Ribeiro  RR, Tafuri  WL, Melo  MN, Michalick  MSM. First report of vertical transmission of Leishmania (Leishmania) infantum in a naturally infected bitch from Brazil. Vet Parasitol. 2009;166:15962. DOIPubMedGoogle Scholar
  12. Mancianti  F, Sozzi  S. Isolation of Leishmania from a newborn puppy. Trans R Soc Trop Med Hyg. 1995;89:402. DOIPubMedGoogle Scholar
  13. Pangrazio  KK, Costa  EA, Amarilla  SP, Cino  AG, Silva  TMA, Paixão  TA, et al. Tissue distribution of Leishmania chagasi and lesions in transplacentally infected fetuses from symptomatic and asymptomatic naturally infected bitches. Vet Parasitol. 2009;165:32731. DOIPubMedGoogle Scholar
  14. Masucci  M, De Majo  M, Contarino  RB, Borruto  G, Vitale  F, Pennisi  MG. Canine leishmaniasis in the newborn puppy. Vet Res Commun. 2003;27(Suppl 1):7714. DOIPubMedGoogle Scholar
  15. Naucke  TJ, Lorentz  S. First report of venereal and vertical transmission of canine leishmaniosis from naturally infected dogs in Germany. Parasit Vectors. 2012;5:67. DOIPubMedGoogle Scholar
  16. Galindo-Sevilla  N, Mancilla-Ramírez  J. T-cell tolerance as a potential effect of congenital leishmaniasis on offspring immunity. Parasite Immunol. 2019;41:e12540. DOIPubMedGoogle Scholar
  17. Adam  GK, Omar  SM, Ahmed  MA, Abdallah  TM, Ali  AA. Cross-sectional study of the case-fatality rate among patients with visceral leishmaniasis infections during pregnancy in Sudan. Int J Gynaecol Obstet. 2018;140:11920. DOIPubMedGoogle Scholar
  18. Akopyants  NS, Kimblin  N, Secundino  N, Patrick  R, Peters  N, Lawyer  P, et al. Demonstration of genetic exchange during cyclical development of Leishmania in the sand fly vector. Science. 2009;324:2658. DOIPubMedGoogle Scholar
  19. Inbar  E, Shaik  J, Iantorno  SA, Romano  A, Nzelu  CO, Owens  K, et al. Whole genome sequencing of experimental hybrids supports meiosis-like sexual recombination in Leishmania. PLoS Genet. 2019;15:e1008042. DOIPubMedGoogle Scholar
  20. Figueiró-Filho  EA, El Beitune  P, Queiroz  GT, Somensi  RS, Morais  NO, Dorval  MEC, et al. Visceral leishmaniasis and pregnancy: analysis of cases reported in a central-western region of Brazil. Arch Gynecol Obstet. 2008;278:136. DOIPubMedGoogle Scholar
  21. Pagliano  P, Carannante  N, Rossi  M, Gramiccia  M, Gradoni  L, Faella  FS, et al. Visceral leishmaniasis in pregnancy: a case series and a systematic review of the literature. J Antimicrob Chemother. 2005;55:22933. DOIPubMedGoogle Scholar
  22. Anderson  DC, Buckner  RG, Glenn  BL, MacVean  DW. Endemic canine leishmaniasis. Vet Pathol. 1980;17:946. DOIPubMedGoogle Scholar
  23. Gaskin  AA, Schantz  P, Jackson  J, Birkenheuer  A, Tomlinson  L, Gramiccia  M, et al. Visceral leishmaniasis in a New York foxhound kennel. J Vet Intern Med. 2002;16:3444. DOIPubMedGoogle Scholar
  24. Owens  SD, Oakley  DA, Marryott  K, Hatchett  W, Walton  R, Nolan  TJ, et al. Transmission of visceral leishmaniasis through blood transfusions from infected English foxhounds to anemic dogs. J Am Vet Med Assoc. 2001;219:107683. DOIPubMedGoogle Scholar
  25. Gibson-Corley  KN, Hostetter  JM, Hostetter  SJ, Mullin  K, Ramer-Tait  AE, Boggiatto  PM, et al. Disseminated Leishmania infantum infection in two sibling foxhounds due to possible vertical transmission. Can Vet J. 2008;49:10058.PubMedGoogle Scholar
  26. 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;12:4406. DOIPubMedGoogle Scholar
  27. 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;226:131622. DOIPubMedGoogle Scholar
  28. 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;21:220912. DOIPubMedGoogle Scholar
  29. Duthie  MS, Petersen  C. Could canine visceral leishmaniosis take hold in the UK? Vet Rec. 2019;184:43840. DOIPubMedGoogle Scholar
  30. Rosypal  AC, Zajac  AM, Lindsay  DS. Canine visceral leishmaniasis and its emergence in the United States. [viii.] [viii.]. Vet Clin North Am Small Anim Pract. 2003;33:92137, viii. DOIPubMedGoogle Scholar
  31. Larson  M, Toepp  A, Scott  B, Kurtz  M, Fowler  H, Esfandiari  J, et al.; EPID:158:001. Semi-quantitative measurement of asymptomatic L. infantum infection and symptomatic visceral leishmaniasis in dogs using Dual-Path Platform® CVL. Appl Microbiol Biotechnol. 2017;101:38190. DOIPubMedGoogle Scholar
  32. Li  H, Durbin  R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics. 2009;25:175460. DOIPubMedGoogle Scholar
  33. Van der Auwera  GA, Carneiro  MO, Hartl  C, Poplin  R, Del Angel  G, Levy-Moonshine  A, et al. From FastQ data to high confidence variant calls: the Genome Analysis Toolkit best practices pipeline. Curr Protoc Bioinformatics. 2013;43:11.10.1–33.
  34. Pembleton  LW, Cogan  NOI, Forster  JW. StAMPP: an R package for calculation of genetic differentiation and structure of mixed-ploidy level populations. Mol Ecol Resour. 2013;13:94652. DOIPubMedGoogle Scholar
  35. Kozlov  AM, Darriba  D, Flouri  T, Morel  B, Stamatakis  A. RAxML-NG: a fast, scalable and user-friendly tool for maximum likelihood phylogenetic inference. Bioinformatics. 2019;35:44535. DOIPubMedGoogle Scholar
  36. Alexander  DH, Novembre  J, Lange  K. Fast model-based estimation of ancestry in unrelated individuals. Genome Res. 2009;19:165564. DOIPubMedGoogle Scholar
  37. Britton  T, Anderson  CL, Jacquet  D, Lundqvist  S, Bremer  K. Estimating divergence times in large phylogenetic trees. Syst Biol. 2007;56:74152. DOIPubMedGoogle Scholar
  38. Franssen  SU, Durrant  C, Stark  O, Moser  B, Downing  T, Imamura  H, et al. Global genome diversity of the Leishmania donovani complex. eLife. 2020;9:e51243. DOIPubMedGoogle Scholar
  39. Carnielli  JBT, Crouch  K, Forrester  S, Silva  VC, Carvalho  SFG, Damasceno  JD, et al. A Leishmania infantum genetic marker associated with miltefosine treatment failure for visceral leishmaniasis. EBioMedicine. 2018;36:8391. DOIPubMedGoogle Scholar
  40. Peacock  CS, Seeger  K, Harris  D, Murphy  L, Ruiz  JC, Quail  MA, et al. Comparative genomic analysis of three Leishmania species that cause diverse human disease. Nat Genet. 2007;39:83947. DOIPubMedGoogle Scholar
  41. Danecek  P, Auton  A, Abecasis  G, Albers  CA, Banks  E, DePristo  MA, et al.; 1000 Genomes Project Analysis Group. The variant call format and VCFtools. Bioinformatics. 2011;27:21568. DOIPubMedGoogle Scholar
  42. Quinlan  AR, Hall  IM. BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics. 2010;26:8412. DOIPubMedGoogle Scholar
  43. Kofler  R, Pandey  RV, Schlötterer  C. PoPoolation2: identifying differentiation between populations using sequencing of pooled DNA samples (Pool-Seq). Bioinformatics. 2011;27:34356. DOIPubMedGoogle Scholar
  44. Teixeira  DG, Monteiro  GRG, Martins  DRA, Fernandes  MZ, Macedo-Silva  V, Ansaldi  M, et al. Comparative analyses of whole genome sequences of Leishmania infantum isolates from humans and dogs in northeastern Brazil. Int J Parasitol. 2017;47:65565. DOIPubMedGoogle Scholar
  45. Kuhls  K, Chicharro  C, Cañavate  C, Cortes  S, Campino  L, Haralambous  C, et al. Differentiation and gene flow among European populations of Leishmania infantum MON-1. PLoS Negl Trop Dis. 2008;2:e261. DOIPubMedGoogle Scholar
  46. Leblois  R, Kuhls  K, François  O, Schönian  G, Wirth  T. Guns, germs and dogs: On the origin of Leishmania chagasi. Infect Genet Evol. 2011;11:10915. DOIPubMedGoogle Scholar
  47. Dumetz  F, Imamura  H, Sanders  M, Seblova  V, Myskova  J, Pescher  P, et al. Modulation of aneuploidy in Leishmania donovani during adaptation to different in vitro and in vivo environments and its impact on gene expression. MBio. 2017;8:e0059917. DOIPubMedGoogle Scholar
  48. Franssen  SU, Takele  Y, Adem  E, Sanders  MJ, Müller  I, Kropf  P, et al. Diversity and within-host evolution of Leishmania donovani from visceral leishmaniasis patients with and without HIV coinfection in northern Ethiopia. MBio. 2021;12:e0097121. DOIPubMedGoogle Scholar
  49. 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

Main Article

1These senior authors contributed equally to this article.

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