Parasitology Research

, Volume 112, Issue 8, pp 2913–2923 | Cite as

Effect of lipopolysaccharide (LPS) from Ochrobactrum intermedium on sheep experimentally infected with Fasciola hepatica

  • J. M. Martínez-Pérez
  • D. Robles-Pérez
  • F. Valcárcel-Sancho
  • A. M. González-Guirado
  • I. Casanova-García de Castro
  • J. M. Nieto-Martínez
  • F. A. Rojo-Vázquez
  • M. Martínez-Valladares
Original Paper

Abstract

The effects of the lipopolysaccharide (LPS) from Ochrobactrum intermedium was evaluated in sheep experimentally infected with Fasciola hepatica. Animals were divided into four groups: two treated with the LPS (T1/T2) and two controls (C1/C2). T1/C1 were slaughtered at 30 days postinfection (dpi) and T2/C2 at 85 dpi. Body weight and body condition were found higher in T1 and T2 than in controls, although differences were not significant. Treated sheep showed lower cumulative fecal egg count than controls (p < 0.01). Levels of red blood cells (RBC), white blood cells, hemoglobin, and hematocrit (HCT) were higher in T1 and T2. Significant differences (p < 0.05) in RBC and HCT were found between groups at 84 dpi. More severe macrocytic and hypochromic anemia was observed in C1 and C2 than in treated groups. Total protein and albumin values were higher in T1 and T2 (p < 0.01) until 29 dpi. At the end of the trial, no significant differences were observed in hepatic enzymes, although gamma-glutamyl transferase and aspartate aminotransferase values were higher in C2, and alanine aminotransferase was higher in T2. At necropsy, the mean weight of liver, fibrosis in portal triads, and ganglion size were similar in all groups. The number and size of flukes was greater in C2 than in T2 (p < 0.05). The histological examinations revealed a higher degree of parenchymatous fibrosis in T2 compared to C2 (p < 0.05). The administration of LPS from O. intermedium increased the nonspecific resistance against F. hepatica in experimentally infected sheep.

Notes

Acknowledgments

This research has been supported by Laboratorios Ovejero, S.A., León (Spain). María Martínez-Valladares was supported by a postdoctoral Jae-Doc contract from the Consejo Superior de Investigaciones Científicas (CSIC) and co-funded by the European social fund.

References

  1. Abel LCJ, Chen S, Ricca LG, Martins MF, García M, Ananías RZ, Mussalem JS, Squaiella CC, Shaw RJ, Longo-Maugéri IM (2009) Adjuvant effect of LPS and killed Propionibacterium acnes on the development of experimental gastrointestinal nematode infestation in sheep. Parasite Immunol 31:604–612PubMedCrossRefGoogle Scholar
  2. Álvarez-Sánchez MÁ, Mainar-Jaime RC, Pérez-García J, Rojo-Vázquez FA (2006) Resistance of Fasciola hepatica to triclabendazole and albendazole in sheep in Spain. Vet Rec 159:424–425PubMedCrossRefGoogle Scholar
  3. Behm CA, Sangster NC (1999) Pathology, pathophysiology, and clinical aspects. In: Dalton JP (ed) Fasciolosis. CAB International, Wallingford, p 198Google Scholar
  4. Benjamín MM (1984) Manual de parasitología clínica veterinaria. México, Limusa editorial, p 135Google Scholar
  5. Brennan GP, Fairweather I, Trudgett A, Hoey E, McCoy MCM, Meaney M, Robinson M, McFerran N, Ryan L, Lanusse C, Mottier L, Álvarez L, Solana H, Virkel G, Brophy PM (2007) Understanding triclabendazole resistance. Exp Mol Pathol 82:104–109PubMedCrossRefGoogle Scholar
  6. Buffoni L, Zafra R, Pérez-Écija A, Martínez-Moreno FJ, Martínez-Galisteo E, Moreno T, Pérez J, Martínez-Moreno Á (2010) Immune response of goats immunized with glutathione S-transferase and experimentally challenged with Fasciola hepatica. Parasitology Int 59:147–153CrossRefGoogle Scholar
  7. Burke MD (2002) Liver function: test selection and interpretation of results. Clin Lab Med 22:377–390PubMedCrossRefGoogle Scholar
  8. Clery D, Torgerson P, Mulcahy G (1996) Immune responses of chronically infected adult cattle to Fasciola hepatica. Vet Parasitol 62:71–82PubMedCrossRefGoogle Scholar
  9. Coffman RL, Sher A, Seder RA (2010) Vaccine adjuvants: putting innate immunity to work. Immunity 33:492–503PubMedCrossRefGoogle Scholar
  10. Cordero del Campillo M, Rojo-Vázquez FA (coords) (1999) Parasitología Veterinaria. Madrid, Interamericana editorialGoogle Scholar
  11. Dalton JP, Mulcahy G (2001) Parasite vaccines – a reality? Vet Parasitol 98:149–167PubMedCrossRefGoogle Scholar
  12. Dalton JP, McConigle S, Rolph TP, Andrews SJ (1996) Induction of protective immunity in cattle against infection with Fasciola hepatica by vaccination with cathepsin L proteinases and with hemoglobin. Infect Immun 64:5066–5074PubMedGoogle Scholar
  13. Dalton JP, Neill SO, Stack C, Collins P, Walshe A, Sekiya M, Doyle S, Mulcahy G, Hoyle D, Khaznadji E, Moiré N, Brennan G, Mousley A, Kreshchenko N, Maule AG, Donnelly SM (2003) Fasciola hepatica cathepsin L-like proteases: biology, function, and potential in the development of first generation liver fluke vaccines. Int J Parasitol 33:1173–1181PubMedCrossRefGoogle Scholar
  14. Dreisbach VC, Cowley S, Elkins KL (2000) Purified lipopolysaccharide from Francisella tularensis live vaccine strain (LVS) induces protective immunity against LVS infection that requires B cells and gamma interferon. Infect Immun 68:1988–1996PubMedCrossRefGoogle Scholar
  15. Erroi A, Fantuzzi G, Mengozzi M, Sironi M, Orencole SF, Clark BD, Dinarello CA, Isetta A, Gnocchi P, Giovarelli M (1993) Differential regulation of cytokine production in lipopolysaccharide tolerance in mice. Infect Immun 61:4356–4359PubMedGoogle Scholar
  16. Fairweather I (2005) Triclabendazole: new skills to unravel and old(ish) enigma. J Helminthol 79:227–234PubMedCrossRefGoogle Scholar
  17. Ferre I, Barrio JP, González-Gallego J, Rojo-Vázquez FA (1994) Appetite depression in sheep experimentally infected with Fasciola hepatica L. Vet Parasitol 55:71–79PubMedCrossRefGoogle Scholar
  18. Ferre I, López P, Rojo-Vázquez FA, González-Gallego J (1996) Experimental ovine fasciolosis: antipyrine clearance as indicator of liver damage. Vet Parasitol 62:93–100PubMedCrossRefGoogle Scholar
  19. Haçariz O, Sayers G, McCullough M, Garrett M, O´Donovan J, Mulcahy G (2009) The effect of Quil A adjuvant on the course of experimental Fasciola hepatica infection in sheep. Vaccine 27:45–50PubMedCrossRefGoogle Scholar
  20. Haroun E, Hillyer GV (1986) Resistance to fascioliasis: a review. Vet Parasitol 20:63–70PubMedCrossRefGoogle Scholar
  21. Kaneko J (1980) Clinical biochemistry of domestic animals. Academic, New YorkGoogle Scholar
  22. Kesik M, Jedlina-Panasiuk L, Kozak-Cieszczyk M, Plucienniczak A, Wedrychowicz H (2007) Enteral vaccination of rats against Fasciola hepatica using recombinant cysteine proteinase (cathepsin L1). Vaccine 25:3619–3628PubMedCrossRefGoogle Scholar
  23. López-Abán J, Ramajo V, Pérez-Arellano JL, Oleaga A, Hillyer GV, Muro A (1999) A fatty acid binding protein from Fasciola hepatica induced protection in C57/B1 mice from challenge infection with Schistosoma bovis. Vet Parasitol 83:107–121CrossRefGoogle Scholar
  24. Martínez-Moreno Á, Jiménez-Luque V, Moreno T, Redondo ESH, Martín de las Mulas J, Pérez J (1999) Liver pathology and immune response in experimental Fasciola hepatica infections of goats. Vet Parasitol 82:19–33Google Scholar
  25. Martínez-Valladares M, Cordero-Pérez C, Castañón-Ordóñez L, Famularo MR, Fernández-Pato N, Rojo-Vázquez FA (2010a) Efficacy of a moxidectin/triclabendazole oral formulation against mixed infections of Fasciola hepatica and gastrointestinal nematodes in sheep. Vet Parasitol 174:166–169PubMedCrossRefGoogle Scholar
  26. Martínez-Valladares M, Famularo MR, Fernández-Pato N, Castañón-Ordóñez L, Cordero-Pérez C, Rojo-Vázquez FA (2010b) Efficacy of nitroxynil against Fasciola hepatica resistant to triclabendazole in a naturally infected sheep flock. Parasitol Res 107:1205–1211PubMedCrossRefGoogle Scholar
  27. Masihi KN (2000) Immunomodulators in infectious diseases: panoply of possibilities. Int J Immunopharmacol 22:1083–1091PubMedCrossRefGoogle Scholar
  28. Masihi KN, Lange W (1988) Immunomodulators and nonspecific host defense mechanisms against microbial infections. Pergamon Press, New York, pp 1–462Google Scholar
  29. Massoud A, El Sisi S, Salama O, Massoud A (2001) Preliminary study of therapeutic efficacy of a new fasciolicidal drug derived from Commiphora molmol (MYRRH). AmJTrop Med Hyg 65:96–99Google Scholar
  30. McConville M, Brennan GP, Flanagan A, Edgar HW, Hanna RE, McCoy M, Gordon AW, Castillo R, Hernández-Campos A, Fairweather I (2009) An evaluation of the efficacy of compound alpha and triclabendazole against two isolates of Fasciola hepatica. Vet Parasitol 162:75–88PubMedCrossRefGoogle Scholar
  31. Mendes RE, Pérez-Écija RA, Zafra R, Buffoni L, Martínez-Moreno Á, Dalton JP, Mulcahy G, Pérez J (2010a) Evaluation of hepatic changes and local and systemic immune responses in goats immunized with recombinant Peroxiredoxin (Prx) and challenged with Fasciola hepatica. Vaccine 28:2832–2840PubMedCrossRefGoogle Scholar
  32. Mendes RE, Zafra R, Pérez-Écija RA, Buffoni L, Martínez-Moreno Á, Tendler M, Pérez J (2010b) Evaluation of local immune response to Fasciola hepatica experimental infection in the liver and hepatic lymph nodes of goats immunized with Sm14 vaccine antigen. Mem Inst Oswaldo Cruz 105:698–705PubMedCrossRefGoogle Scholar
  33. Morrison CA, Colin T, Sexton JL, Bowen F, Wicker J, Friedel T, Spithill TW (1996) Protection of cattle against Fasciola hepatica infection by vaccination with glutathione S-transferase. Vaccine 14:1603–1612PubMedCrossRefGoogle Scholar
  34. Mulcahy G, Dalton JP (2001) Cathepsin L proteinases as vaccines against infection with Fasciola hepatica (liver fluke) in ruminants. Res Vet Sci 70:83–86PubMedCrossRefGoogle Scholar
  35. Muro A, Ramajo V, López J, Simón F, Hillyer GV (1997) Fasciola hepatica: vaccination of rabbits with native and recombinant antigens related to fatty acid binding proteins. Vet Parasitol 69:219–229PubMedCrossRefGoogle Scholar
  36. Nicholls EF, Madera L, Hancock REW (2010) Immunomodulators as adjuvants for vaccines and antimicrobial therapy. Ann N Y Acad Sci 1213:46–61PubMedCrossRefGoogle Scholar
  37. Ovejero-Guisasola JI, Fresno-Escudero M (2010) Lipopolysaccharide of Ochrobactrum intermedium and their use as immunostimulant of mammalians. WO 2010/139352 A1Google Scholar
  38. Overend DJ, Bowen FL (1995) Resistance of Fasciola hepatica to triclabendazole. Aust Vet J 72:275–276PubMedCrossRefGoogle Scholar
  39. Piacenza L, Acosta D, Basmadjian I, Dalton JP, Carmona C (1999) Vaccination of sheep with cathepsin L proteinases and with leucine aminopeptidase induces high levels of protection against fasciolosis. Infect Immun 67:1954–1961PubMedGoogle Scholar
  40. Prichard R (1994) Anthelmintic resistance. Vet Parasitol 64:259–268CrossRefGoogle Scholar
  41. Pullan NB, Sewell MMH, Hammond JA (1970) Studies on the pathogenicity of massive infections of Fasciola hepatica L. in lambs. Brit Vet J 126:543–558Google Scholar
  42. Rietschel ET, Brade H (1992) Bacterial endotoxins. Sci Am 267:54–61PubMedCrossRefGoogle Scholar
  43. Russel AJF, Doney JM, Gunn RG (1969) Subjective assessment of body fat in live sheep. J Agr Sci 72:451–454CrossRefGoogle Scholar
  44. Schalm O, Jain J, Carroll E (1981) Hematología Veterinaria. Buenos Aires, Hemisferio SurGoogle Scholar
  45. Severin K, Masek T, Janicki Z, Konjevic D, Slavica A, Marinculic A, Martinkovic F, Vengust G, Dzaja P (2012) Liver enzymes and blood metabolites in a population of free-ranging red deer (Cervus elaphus) naturally infected with Fascioloides magna. J Helminthol 86:190–196PubMedCrossRefGoogle Scholar
  46. Sexton JL, Milner AR, Panaccio M, Waddington J, Wijffels G, Chandler D, Thompson C, Wilson L, Spithill TW, Mitchell GF (1990) Glutathione S-transferase novel vaccine against Fasciola hepatica infection in sheep. J Immunol 145:3905–3910PubMedGoogle Scholar
  47. Sykes AR, Coop RL, Robinson M (1980) Chronic subclinical ovine fasciolosis: plasma glutamate dehydrogenase, gamma-glutamyl transpeptidase and aspartate aminotransferase activities and their significance as diagnostic aids. Res Vet Sci 28:71–75PubMedGoogle Scholar
  48. Talukder S, Bhuiyan MJ, Hossain MM, Uddin MM, Paul S, Howlader MMR (2010) Pathological investigation of liver fluke infection of slaughtered Black Bengal goat in a selected area of Bangladesh. Bang J Vet Med 8:35–40Google Scholar
  49. Thienpont D, Rochette F, Vanparijs OFJ (1986) Diagnosing helminthiasis by coprological examination. Beerse, Janssen Research Foundation, pp. 40–41Google Scholar
  50. Van der Ley P (2001) Modification of lipid A biosynthesis in Neisseria meningitidis lpxL mutants: influence on lipopolysaccharide structure, toxicity, and adjuvant activity. Infect Immun 69:5981–5990PubMedCrossRefGoogle Scholar
  51. Van Milligen FJ, Cornelissen JBWJ, Hendriks IM, Gaasenbeek CPH, Bokhout BA (1998) Protection to Fasciola hepatica in the gut mucosa of immune rats is associated with infiltrates of eosinophils, IgG1, and IgG2a antibodies around the parasites. Parasite Immunol 20:285–292PubMedCrossRefGoogle Scholar
  52. Vercruysse J, Dorny P, Hong C, Harris TJ, Hammet NC, Smith DG, Weatherley AJ (1993) Efficacy of doramectin in the prevention of gastrointestinal nematode infections in grazing cattle. Vet Parasitol 49:51–59PubMedCrossRefGoogle Scholar
  53. Veremeichenko SN, Zdorovenko GM (2008) Specific structural features and immunomodulatory properties of the lipopolysaccharides of Pseudomonas bacteria. Appl Biochem Microbiol 44:571–579CrossRefGoogle Scholar
  54. Vuopio-Varkila J, Marjatta N, Pyhälä L, Mäkelä PH (1988) Lipopolysaccharide-induced nonspecific resistance to systemic Escherichia coli infection in mice. J Med Microbiol 25:197–203PubMedCrossRefGoogle Scholar
  55. Zafra R, Buffoni L, Pérez-Écija RA, Mendes RE, Martínez-Moreno Á, Martínez-Moreno FJ, Pérez J (2009) Study of the local immune response to Fasciola hepatica in the liver and hepatic lymph nodes of goats immunized with a peptide of the Sm14 antigen. Res Vet Sci 87:226–232PubMedCrossRefGoogle Scholar
  56. Zafra R, Pérez-Écija RA, Buffoni L, Mendes RE, Martínez-Moreno Á, Martínez-Moreno FJ, Martínez-Galisteo ME, Pérez J (2010) Evaluation of hepatic damage and local immune response in goats immunized with native Glutathione S-transferase of Fasciola hepatica. J Comp Pathol 143:110–119PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • J. M. Martínez-Pérez
    • 1
  • D. Robles-Pérez
    • 1
  • F. Valcárcel-Sancho
    • 2
  • A. M. González-Guirado
    • 2
  • I. Casanova-García de Castro
    • 2
  • J. M. Nieto-Martínez
    • 2
  • F. A. Rojo-Vázquez
    • 1
    • 3
  • M. Martínez-Valladares
    • 3
  1. 1.Facultad de VeterinariaUniversidad de LeónLeonSpain
  2. 2.Centro de Investigación en Sanidad Animal (CISA-INIA)MadridSpain
  3. 3.Instituto de Ganadería de Montaña (CSIC-ULE), Finca de MarzanasLeonSpain

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