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Occurrence, prevalence, and explanatory environmental variables of Spirocerca vulpis infestation in the foxes of western Spain

  • M. Martín-Pérez
  • J.M. Lobo
  • J.E. Pérez-Martín
  • D. Bravo-Barriga
  • J. Galapero
  • E. FronteraEmail author
Helminthology - Original Paper
  • 29 Downloads

Abstract

The main aim of this study was to not only establish the prevalence of the recently described Spirocerca vulpis parasite in the wild-life cycle of carnivores in western Spain but to also elaborate a model to explain the risk of infestation based on 16 topo-climatic and habitat variables. During the period from June 2016 to November 2017, 1644 carcasses of red foxes (Vulpes vulpes) and another 105 wild mammals, legally hunted or killed in car accidents, were analyzed. Parasitic nodules of Spirocerca were found in 6% of the foxes, and the molecular analyses established a homology of our samples with the species S. vulpis. There were no differences in the occurrence of the infestation between sexes, but there were differences in terms of age, such that infestation was proportionally more frequent among young individuals. In terms of temporality, a higher percentage of positive cases was observed during the late-autumn and winter months, especially between December and February. This study provides new data on the factors that predispose S. vulpis infection in the red fox. Model results indicate that a spatial pattern exists in the occurrence and prevalence of this species in the studied area (higher probabilities to the west), and that this pattern seems to mainly be associated with topo-climatic variables.

Keywords

Spirocerca vulpis Red fox Explanatory factors Dung beetles Topo-climatic factors Habitat factors 

Notes

Acknowledgments

This work would not be possible without the collaboration of the hunting preserves’ leadership who agreed to participate in the study. We want to thank Professors Donato Traversa (University of Teramo, Italy) and Antonio Frangipane di Regalbono (University of Padua, Italy) for their help in the molecular analysis. The authors would like to acknowledge the students of the Department of Animal Health, University of Extremadura, for their helpful assistance in processing these samples. This research did not receive any specific grant from funding agencies of the public, commercial, or not-for-profit sectors.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

436_2019_6590_MOESM1_ESM.xlsx (20 kb)
ESM 1 (XLSX 19 kb)

References

  1. Al-Sabi MNS, Hansen MS, Chriél M, Holm E, Larsen G, Enemark HL (2014) Genetically distinct isolates of Spirocerca sp. from a naturally infected red fox (Vulpes vulpes) from Denmark. Vet Parasitol 205:389–396.  https://doi.org/10.1016/j.vetpar.2014.07.002 CrossRefPubMedGoogle Scholar
  2. Aroch I, Markovics A, Mazaki-Tovi M, Kuzi S, Harrus S, Yas E, Baneth G, Bar-El M, Bdolah-Abram T, Segev G, Lavy E (2015) Spirocercosis in dogs in Israel: a retrospective case-control study (2004–2009). Vet Parasitol 211:234–240.  https://doi.org/10.1016/j.vetpar.2015.05.011 CrossRefPubMedGoogle Scholar
  3. Bailey WS (1972) Spirocerca lupi: a continuing Inquiry. J Parasitol 58:3–22CrossRefGoogle Scholar
  4. Bailey WS, Cabrera DJ, Diamond DL (1963) Beetles of the family Scarabaeidae as intermediate hosts for Spirocerca lupi. J Parasitol 49:485–488CrossRefGoogle Scholar
  5. Blancou J, Albignac R, Albignac R (1976) Note sur l’infestation des Lémuriens malgaches par Spirocerca lupi (Rudolphi, 1809). Rev Elev Méd Vét Pays Trop 29(2):127–130CrossRefGoogle Scholar
  6. Bumby MM, Williams MC, Steyl JCA, Harrison-White R, Lutermann H, Fosgate GT, de Waal PJ, Mitha J, Clift SJ (2017) Genotyping and comparative pathology of Spirocerca in black-backed jackals (Canis mesomelas) in South Africa. BMC Vet Res 13:1–9.  https://doi.org/10.1186/s12917-017-1175-4 CrossRefGoogle Scholar
  7. Cabrero-Sañudo F, Trotta-Moureu N, Corra M, Bravo O (2008) Composición de especies y estacionalidad de una comunidad de escarabajos del estiércol (Coleoptera: Scarabaeoidea) de la meseta central de la Península Ibérica. Boletín de la S E A 42:305–315Google Scholar
  8. Carvalho JC, Gomes P (2004) Feeding resource partitioning among four sympatric carnivores in the Peneda-Geres National Park (Portugal). J Zool (Lond) 263:275–283.  https://doi.org/10.1017/S0952836904005266 CrossRefGoogle Scholar
  9. Casiraghi M, Anderson TJ, Bandi C, Bazzocchi C, Genchi C (2001) A phylogenetic analysis of filarial nematodes: comparison with the phylogeny of Wolbachia endosymbionts. Parasitology 122:93–103.  https://doi.org/10.1017/s0031182000007149 CrossRefPubMedGoogle Scholar
  10. Chhabra RC, Singh KS (1972) On the life cycle of Spirocerca lupi: preinfective stages in the intermediate host. J Helminthol 46(2):125–137.  https://doi.org/10.1017/S0022149X00022203 CrossRefPubMedGoogle Scholar
  11. Chikweto A, Bhaiyat MI, Tiwari KP, CDe A, Sharma RN (2012) Spirocercosis in owned and stray dogs in Grenada. Vet Parasitol 190(3–4):613–616.  https://doi.org/10.1016/j.vetpar.2012.07.006 CrossRefPubMedGoogle Scholar
  12. Criado-Fornelio A, Gutierrez-Garcia L, Rodriguez-Caabeiroa F, Reus-Garciab E, Roldan-Sorianob MA, Diaz-Sanchez MA (2000) A parasitological survey of wild red foxes (Vulpes vulpes) from the province of Guadalajara, Spain. Vet Parasitol 92:245–251.  https://doi.org/10.1016/S0304-4017(00)00329-0 CrossRefPubMedGoogle Scholar
  13. Dantas-Torres F, Otranto D (2014) Dogs, cats, parasites, and humans in Brazil: opening the black box. Parasit Vectors 7:22.  https://doi.org/10.1186/1756-3305-7-22 CrossRefPubMedPubMedCentralGoogle Scholar
  14. Diakou A, Karamanavi E, Eberhard M, Diakou A, Karamanavi E, Eberhard M, Kaldrimidou E (2012) First report of Spirocerca lupi infection in red fox Vulpes vulpes in Greece. Wildl Biol 18(3):333–336.  https://doi.org/10.2981/11-094 CrossRefGoogle Scholar
  15. Díaz-Ruiz F, Delibes-Mateos M, Garcia-Moreno JL, Lopez-Martin J, Ferreira C, Ferreras P (2011) Biogeographical patterns in the diet of an opportunistic predator: the red fox Vulpes vulpes in the Iberian Peninsula. Mammal Rev 43(1):59–70CrossRefGoogle Scholar
  16. Dixon KG, McCue JF (1967) Further observations on the epidemiology of Spirocerca lupi in the southeastern United States. J Parasitol 53:1074–1075.  https://doi.org/10.2307/3276842 CrossRefPubMedGoogle Scholar
  17. Dobson AJ, Barnett AG (2018) An introduction to generalized linear models, 4th edn. CRC Press, Boca RatonGoogle Scholar
  18. Domínguez G, de la Torre JA (2002) Aprotaciones al conocimiento de los endoparásitos del lobo ibérico (Canis lupus signatus Cabrera, 1907). Galemys 14:49–58Google Scholar
  19. Du Toit CA, Holter P, Lutermann H, Scholtz CH (2012) Role of dung beetle feeding mechanisms in limiting the suitability of species as hosts for the nematode Spirocerca lupi. Med Vet Entomol 26(4):455–457.  https://doi.org/10.1111/j.1365-2915.2011.01008.x CrossRefPubMedGoogle Scholar
  20. Du Toit CA, Scholtz CH, Hyman WB (2008) Prevalence of the dog nematode Spirocerca lupi in populations of its intermediate dung beetle host in the Tshwane (Pretoria) Metropole, South Africa. Onderstepoort J Vet Res 75(4):315–321PubMedGoogle Scholar
  21. Eira C, Miquel J, Vingada J, Torres J, Eira C, Miquel J, Torres J (2006) Spermiogenesis and spermatozoon ultrastructure of the cestode Mosgovoyia ctenoides (Cyclophyllidea: Anoplocephalidae), an intestinal parasite of Oryctolagus cuniculus (Lagomorpha: Leporidae) parasite of Oryctolagus cuniculus (Lagomorpha: Leporidae). J Parasit Dis 92(4):708–718.  https://doi.org/10.1645/GE-818R.1 CrossRefGoogle Scholar
  22. Felicísimo ÁM, Muñoz J, Villalba J, Mateo RG (2011) Impactos, vulnerabilidad y adaptación al cambio climático de la biodiversidad española. 2. Flora y vegetación. Ed. Oficina española de cambio climático, Ministerio de Medio Ambiente y Medio Rural y Marino. Madrid, EspañaGoogle Scholar
  23. Ferrantelli V, Riili S, Vicari D, Percipalle M, Chetta M, Monteverde V, Gaglio G, Giardina G, Usai F, Poglayen G (2010) Spirocerca lupi isolated from gastric lesions in foxes (Vulpes vulpes) in Sicily (Italy). Pol J Vet Sci 13(3):465–471PubMedGoogle Scholar
  24. Frank K, Krell F, Slade EM, Raine EH, Chiew LY, Schmitt T, Vairappan CS, Walter P, Blüthgen N (2018) Global dung webs: high trophic generalism of dung beetles along the latitudinal diversity gradient. Ecol Lett 21:1229–1236.  https://doi.org/10.1111/ele.13095 CrossRefPubMedGoogle Scholar
  25. Frediani J (1996) Dieta anual del zorro, Vulpes vulpes, en dos hábitats del parque Nacional de Doñana. Doñana Acta Vertebrata 23(2):143–152Google Scholar
  26. Galante E, Mena J, Lumbreras C (1995) Dung beetles (Coleoptera: Scarahaeidae, Geotrupidae) attracted to fresh cattle dung in wooded and open pasture. Environ Entomol 24(5):1063–1068.  https://doi.org/10.1093/ee/24.5.1063 CrossRefGoogle Scholar
  27. Genchi C, Rinaldi L, Mortarino M, Genchi M, Cringoli G (2009) Climate and Dirofilaria infection in Europe. Vet Parasitol 163(4):286–292.  https://doi.org/10.1016/j.vetpar.2009.03.026 CrossRefPubMedGoogle Scholar
  28. Gortázar C (1997) Ecología y patología del zorro (Vulpes vulpes, l.) en el valle medio del Ebro. Tesis Doctoral, Universidad de ZaragozaGoogle Scholar
  29. Gottlieb Y, Klement E, Aroch I, Lavy E, Kaufman M, Samish M, Markovics A (2014) Temporal association of ambient temperature and relative humidity with Spirocerca lupi infection of Onthophagus sellatus: a 14-year longitudinal study. Vet Parasitol 204:238–242.  https://doi.org/10.1016/j.vetpar.2014.05.031 CrossRefPubMedGoogle Scholar
  30. Gottlieb Y, Markovics A, Klement E, Naor S, Samish M, Gottlieb Y, Markovics A, Klement E, Naor S, Samish M, Aroch I, Lavy E (2011) Characterization of Onthophagus sellatus as the major intermediate host of the dog esophageal worm Spirocerca lupi in Israel. Vet Parasitol 180:378–382.  https://doi.org/10.1016/j.vetpar.2011.03.008 CrossRefPubMedGoogle Scholar
  31. Hall T (1999) Bioedit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Se 4:95–98Google Scholar
  32. JyothiSree C, Hafeez M (2013) A study on prevalence of spirocercosis in dogs in certain parts of Andhra Pradesh India. Int J Agric Sci Vet Med 1(3):59–66Google Scholar
  33. Laaksonen S, Pusenius J, Kumpula J, Venäläinen A, Kortet R, Oksanen A, Hoberg E (2010) Climate change promotes the emergence of serious disease outbreaks of Filarioid nematodes. Ecohealth 7(1):7–13.  https://doi.org/10.1007/s10393-010-0308-z CrossRefPubMedPubMedCentralGoogle Scholar
  34. Legendre P, Legendre L (2012) Numerical Ecology. Elsevier, AmsterdamGoogle Scholar
  35. Lobetti R (2000) Survey of the incidence, diagnosis, clinical manifestations and treatment of Spirocerca lupi in South Africa: research communication. J S Afr Vet Assoc 71(1):43–46.  https://doi.org/10.4102/jsava.v71i1.676 CrossRefPubMedGoogle Scholar
  36. Lobetti R (2014) Follow-up survey of the prevalence, diagnosis, clinical manifestations and treatment of Spirocerca lupi in South Africa. J S Afr Vet Assoc 85(1):1–7.  https://doi.org/10.4102/jsava.v85i1.1169 CrossRefGoogle Scholar
  37. Lobo JM, Hortal J, Cabrero-Sañudo FJ (2006) Regional and local influence of grazing activity on the diversity of a semi-arid dung beetle community. Divers Distrib 12:111–123.  https://doi.org/10.1111/j.1366-9516.2006.00194.x CrossRefGoogle Scholar
  38. López-Fernández ML, López FMS (2008) Clasificación bioclimática mundial y cartografía bioclimática de la España peninsular y balear. Serie botánica 17. Servicio de publicaciones de la Universidad de Navarra. Pamplona, pp 279Google Scholar
  39. Lumaret JP, Kadiri N, Bertrand M (1992) Changes in resources: consequences for the dynamics of dung beetle communities. J Appl Ecol 29(2):349–356.  https://doi.org/10.2307/2404504 CrossRefGoogle Scholar
  40. Magi M, Guardone L, Prati MC, Mignone W, Macchioni F, Sperimentale Z (2014) Extraintestinal nematodes of the red fox Vulpes vulpes in north-West Italy. J Helminthol 89(4):506–511.  https://doi.org/10.1017/S0022149X1400025X CrossRefPubMedGoogle Scholar
  41. Martínez F, Hernández S, Calero R, Moreno T (1978) Contribución al conocimiento de los parásitos del zorro (Vulpes vulpes). Rev Ibér Parasitol 38(1–2):207–211Google Scholar
  42. Martínez-Carrasco C, Ruiz de Ybáñez M, Sagarminaga JL, Garijo M, Moreno F, Acosta I, Hernandez S, Alonso F (2007) Parasites of the red fox (Vulpes vulpes Linnaeus, 1758) in Murcia, Southeast Spain. Rev Med Vet 158(7):331–335Google Scholar
  43. Martín-Piera F, Lobo JM (1996) A comparative discussion of trophic preferences in dung beetle communities. Misc Zool 19:13–31Google Scholar
  44. Mazaki-Tovi M, Baneth G, Aroch I, Harrus S, Kass PH, Ben-Ari T, Zur G, Aizenberg I, Bark H, Lavy E (2002) Canine spirocercosis: clinical, diagnostic, pathologic and epidemiologic characteristics. Vet Parasitol 107(3):235–250.  https://doi.org/10.1016/S0304-4017(02)00118-8 CrossRefPubMedGoogle Scholar
  45. Mense MG, Gardiner CH, Moeller RB, Partridge HL, Wilson S (1992) Chronic emesis caused by a nematode induced gastric nodule in a cat. J Am Anim Hosp Assoc 201:597–598Google Scholar
  46. Mukaratirwa S, Pillay E, Munsammy K (2010) Experimental infection of selected arthropods with spirurid nematodes Spirocerca lupi Raillet & Henry, 1911 and Gongylonema ingluvicola Molin, 1857. J Helminthol 84:369–374.  https://doi.org/10.1017/S0022149X10000039 CrossRefPubMedGoogle Scholar
  47. Murray M, Campbell H, Jarrett WHF (1964) Spirocerca lupi in a cheetah. Afr J Ecol 2164.  https://doi.org/10.1111/j.1365-2028.1964.tb00209.x CrossRefGoogle Scholar
  48. Mylonakis ME, Leontides LS, Rallis T, Patsikas M, Papadopoulos El Koutinas AF, Florou M, Fytianou A, Mylonakis ME (2006) Clinical signs and clinicopathologic abnormalities in dogs with clinical spirocercosis: 39 cases (1996–2004). J Am Vet Med Assoc 228:1063–1067.  https://doi.org/10.2460/javma.228.7.1063 CrossRefPubMedGoogle Scholar
  49. National Research Council (NRC) (1982) Nutrient Requirements of Mink and Foxes. In: Nutrient requirements of animals, 2nd edn. The National Academies Press, Washington, DC.  https://doi.org/10.17226/1114
  50. Ndiritu CG, Al-Sadi HI (1976) Pathogenesis and lesions of canine spirocercosis. Mod Vet Pract 57:924–931PubMedGoogle Scholar
  51. Pence DB, Stone JE (1978) Visceral lesions in wild carnivores naturally infected with Spirocerca lupi. Vet Pathol 15:322–331.  https://doi.org/10.1177/030098587801500306 CrossRefPubMedGoogle Scholar
  52. Popiołek M, Szczęsna-Staśkiewicz J, Bartoszewicz M, Okarma H, Smalec B, Zalewski A (2011) Helminth parasites of an introduced invasive sarnivore species, the raccoon (Procyon lotor L.), from the Warta Mouth National Park (Poland). J Parasitol 97(2):357–360.  https://doi.org/10.1645/ge-2525.1 CrossRefPubMedGoogle Scholar
  53. Rinas MA, Nesnek R, Kinsella JM, Dematteo KE (2009) Fatal aortic aneurysm and rupture in a neotropical bush dog (Speothos venaticus) caused by Spirocerca lupi. Vet Parasitol 164(2–4):347–349.  https://doi.org/10.1016/j.vetpar.2009.05.006 CrossRefPubMedGoogle Scholar
  54. Rojas A, Dvir E, Farkas R, Sarma K, Borthakur S, Jabbar A, Markovics A, Otranto D, Baneth G (2018b) Phylogenetic analysis of Spirocerca lupi and Spirocerca vulpis reveal high genetic diversity and intra-individual variation. Parasit Vectors 11(1):639.  https://doi.org/10.1186/s13071-018-3202-0 CrossRefPubMedPubMedCentralGoogle Scholar
  55. Rojas A, Freedberg N, Markovics A, Gottlieb Y, Baneth G (2017) Influence of physical and chemical factors on the embryonation, hatching and infectivity of Spirocerca lupi. Vet Parasitol 242:71–78.  https://doi.org/10.1016/j.vetpar.2017.05.026 CrossRefPubMedGoogle Scholar
  56. Rojas A, Sanchis-Monsonís G, Alic A, Hodzic A, Otranto D, Yasur-Landau D, Martínez-Carrasco C, Baneth G (2018a) Spirocerca vulpis sp. nov. (Spiruridae: Spirocercidae): description of a new nematode species of the red fox, Vulpes vulpes (Carnivora: Canidae). Parasitology 145(14):1917–1928.  https://doi.org/10.1017/S0031182018000707 CrossRefPubMedGoogle Scholar
  57. Sáenz de Buruaga M, Lucio AJ, Purroy FJ (2001) Reconocimiento de sexo y edad en especies cinegéticas, Edilesa Ed, León, Spain Google Scholar
  58. Sanchis-Monsonís G (2015) Parasitofauna del zorro (Vulpes vulpes) en la Comunidad Valenciana. Tesis Doctoral, Universidad de Murcia, SpainGoogle Scholar
  59. Sanchis-Monsonís G, Fanelli A, Tizzani P, Martínez-Carrasco C (2019) First epidemiological data on Spirocerca vulpis in the red fox: a parasite of clustered geographical distribution. Vet Parasitol Reg Stud Reports 18:100338.  https://doi.org/10.1016/j.vprsr.2019.100338 CrossRefPubMedGoogle Scholar
  60. Santos MJ, Pinto BM, Santos-Reis M (2007) Trophic niche partitioning between two native and two exotic carnivores in SW Portugal. Web Ecol 7(1):53–62.  https://doi.org/10.5194/we-7-53-2007 CrossRefGoogle Scholar
  61. Sasani F, Javanbakht J, Javaheri A, Mohammad Hassan MA, Bashiri S (2012) The evaluation of retrospective pathological lesions on spirocercosis (Spirocerca lupi) in dogs. J Parasit Dis 38:170–173.  https://doi.org/10.1007/s12639-012-0216-y CrossRefPubMedPubMedCentralGoogle Scholar
  62. Segovia JM, Torres J, Miquel J (2004) Helminth parasites of the red fox (Vulpes vulpes L., 175) in the Iberian Peninsula: an ecological study. Acta Parasitol 49(1):67–79Google Scholar
  63. Serafini P, Lovari S (1993) Food habits and trophic niche overlap of the red fox and the stone marten in a Mediterranean rural area. Acta Theriol 38(3):233–244CrossRefGoogle Scholar
  64. Sprent P, Smeeton NC (2007) Applied nonparametric statistical methods, 4th edn. CRC Press, Boca RatonGoogle Scholar
  65. Szafrańska E, Wasielewski O, Bereszynski A (2007) A faecal analysis of helminth infections in wild and captive wolves, Canis lupus L., in Poland. J Helminthol 84:415–419.  https://doi.org/10.1017/S0022149X10000106 CrossRefGoogle Scholar
  66. Szczęsna J, Popiołek M (2007) The first record of Spirocerca lupi (Rudolphi, 1809) (Spirocercidae, Nematoda) from Poland based on faecal analysis of wolf (Canis lupus L.). Helminthol 44(4):230–232.  https://doi.org/10.2478/s11687-007-0038-0 CrossRefGoogle Scholar
  67. Urquhart GM, Armour J, Duncan JL, Dunn AM, Jennings FW (1996) Veterinary parasitology, 2nd edn. Blackwell Science Ltd., Oxford, p 307 https://trove.nla.gov.au/version/46512203 Google Scholar
  68. Valcárcel F, González J, Aguilar A, Sánchez M, González MG, Suárez R, Tercero AM, Tercero JM, Nieto JM, González-guirado AM, Olmeda AS (2018) Spirocercosis in red fox (Vulpes vulpes) in a natural reserve located in a meso-Mediterranean area. Vet Parasitol Reg Stud Reports 13:115–119.  https://doi.org/10.1016/j.vprsr.2018.05.002 CrossRefPubMedGoogle Scholar
  69. Valencia-Barrera RM, Comtois P, Fernández-González D (2002) Bioclimatic indices as a tool in pollen forecasting. Int J Biometeorol 46:171–175.  https://doi.org/10.1007/s00484-002-0138-y CrossRefPubMedGoogle Scholar
  70. Van der Merwe LL, Kirberger RM, Clift S, Williams M, Keller N, Naidoo V (2008) Spirocerca lupi infection in the dog: a review. Vet J 176:294–309.  https://doi.org/10.1016/j.tvjl.2007.02.032 CrossRefPubMedGoogle Scholar
  71. Voigt DR, Macdonald DW (1984) Variation in the spatial and social behaviour of the red fox, Vulpes vulpes. Acta Zool Fenn 171:261–265Google Scholar
  72. Wandera JG (1976) Further observations on canine spirocercosis in Kenya. Vet Rec 99:348–351.  https://doi.org/10.1136/vr.99.18.348 CrossRefPubMedGoogle Scholar
  73. Warton DI, Hui FKC (2011) The arcsine is asinine: the analysis of proportions in ecology. Ecology 92(1):3–10.  https://doi.org/10.1890/10-0340.1 CrossRefPubMedGoogle Scholar
  74. Webster P, Monrad J, Kapel CMO, Kristensen AT, Jensen AL, Thamsborg SM (2017) The effect of host age and inoculation dose on infection dynamics of Angiostrongylus vasorum in red foxes (Vulpes vulpes). Parasit Vectors 10:4.  https://doi.org/10.1186/s13071-016-1940-4 CrossRefPubMedPubMedCentralGoogle Scholar
  75. Zapata SC, Travaini A, Delibes M (1997) Reproduction of the red fox Vulpes vulpes in Doñana, southern Spain. Mammalia 61:628–631Google Scholar

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Authors and Affiliations

  1. 1.Department of Animal Health, Veterinary FacultyUniversity of ExtremaduraCáceresSpain
  2. 2.Department of Biogeography and Global ChangeMuseo Nacional de Ciencias Naturales (CSIC)MadridSpain
  3. 3.Department of Animal Medicine, Veterinary FacultyUniversity of ExtremaduraCáceresSpain

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