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Acute-phase responses in cattle infected with hydatid cysts and microbial agents

Published online by Cambridge University Press:  13 May 2014

A. Sevimli ,
F.K. Sevimli ,
E. Şeker ,
A. Ulucan  and
H.H. Demirel
A. Sevimli*
Affiliation:
Department of Pathology, Faculty of Veterinary Medicine, Afyon Kocatepe University, Afyonkarahisar, Turkey
F.K. Sevimli
Affiliation:
Department of Parasitology, Faculty of Veterinary Medicine, Afyon Kocatepe University, Afyonkarahisar, Turkey
E. Şeker
Affiliation:
Department of Microbiology, Faculty of Veterinary Medicine, Afyon Kocatepe Üniversity, Afyonkarahisar, Turkey
A. Ulucan
Affiliation:
Department of Pathology Laboratory Techniques, Vocational School of Health Services, Bingol University, Bingol, Turkey
H.H. Demirel
Affiliation:
Department of Pathology, Faculty of Veterinary Medicine, Afyon Kocatepe University, Afyonkarahisar, Turkey
*
* Fax: +90 272 2281349 E-mail: alpers@aku.edu.tr
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Abstract

The aim of this study was to investigate the effect of hydatid cysts and microbial agents on the acute-phase response in cattle. Twenty-seven cattle with hydatid cysts and eight apparently healthy cattle comprised the study and control groups, respectively. Parasitological, microbiological, histopathological and immunohistochemical examinations of the liver and lungs were undertaken, and 49 of these organs were infected with cysts. In 14 of 31 (45.1%) livers and 10 of 18 (55.5%) lungs microbial growth was observed. The most frequent species occurring in the liver were Staphylococcus aureus, Escherichia coli, Corynebacterium spp. and Campylobacter spp., whereas in the lungs the most common species was Candida spp., followed by Streptococcus spp., Mannheimia haemolytica, Corynebacterium spp., Micrococcus spp. and S. aureus. The concentration of serum interleukin (IL-6) in infected cattle, 455.35 ± 39.68 pg/ml, was significantly higher than that of 83.02 ± 17.87 pg/ml in the control group (P< 0.001). The serum amyloid A (SAA) level of infected cattle was 7.51 ± 0.41 μg/ml, and 4.84 ± 0.51 μg/ml in the control group (P< 0.001). The serum haptoglobin level of infected cattle was found to be 2.08 ± 0.65 ng/ml, while that of the control group was determined as 3.87 ± 0.91 ng/ml (P>0.05). The highest concentrations of IL-6 were detected in serum of the cattle where microbial growth had been detected, followed by cattle infected with bacteria + Trichostrongylus sp. (P< 0.001). Consequently, SAA showed an important increase in the group infected with hydatid cysts, whereas haptoglobin level decreased. It was noticed that IL-6, like SAA, had a significant role in hydatid cyst infection. Therefore IL-6 and SAA appear to be major markers in the detection of infection of cattle with hydatid cysts.

Type
Research Papers
Information
Journal of Helminthology , Volume 89 , Issue 4 , July 2015 , pp. 471 - 479
Copyright
Copyright © Cambridge University Press 2014 

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References

Abendaño, N., Juste, R.A. & Alonso-Hearn, M. (2013) Anti-inflammatory and antiapoptotic responses to infection: a common denominator of human and bovine macrophages infected with Mycobacterium avium subsp. paratuberculosis. BioMed Research International 2013, 1–7.CrossRefGoogle ScholarPubMed
Ali, S.A. & Dawood, K.A. (2012) Hydatidosis of cattle with secondary bacterial invaders. Kufa Journal for Veterinary Medical Sciences 3, 104–110.CrossRefGoogle Scholar
Allen, J.E. & Maizels, R.M. (1996) Immunology of human helminth infection. International Archives of Allergy and Immunology 109, 3–10.CrossRefGoogle ScholarPubMed
Al-Qaoud, K.M. & Abdel-Hafez, S.K. (2008) The induction of T helper type 1 response by cytokine gene transfection protects mice against secondary hydatidosis. Parasitology Research 102, 1151–1155.CrossRefGoogle ScholarPubMed
Alsemgeest, S.P.M., Kalsbeek, H.C., Wensing, T.H., van Der Kolk, J.H., van Ederen, A.M., Kim, D.H., Westers, P. & Gruys, E. (1994) The diagnostic value of acute phase proteins in bovine clinical chemistry – a comparison with standard hematological variables. pp. 39–53 in Alsemgeest, S.P.M. Blood concentrations of acute-phase proteins in cattle as markers for disease. Thesis, University of Utrecht, The Netherlands.Google Scholar
Alsemgeest, S.P.M., Lambooy, I.E., Wierenga, H.K., Dieleman, S.J., Meerkerk, B., van Ederen, A.M. & Niewold, T.A. (1995) Influence of physical stress on the plasma concentration of serum amyloid A (SAA) and haptoglobin (HP) in calves. Veterinary Quarterly 17, 9–12.CrossRefGoogle Scholar
Arıdoğan, B.C., Kaya, S., Çetin, E.S., Taş, T. & Demirci, M. (2009) Evaluation of eosinophil cationic protein levels with clinical symptoms and laboratory findings of patients with cystic echinococcosis. Bulletin of Microbiology 43, 285–292.Google Scholar
Aslam, F., Bhaila, I., Nadeem, N. & Fadoo, Z. (2005) Salmonella typhi-infected lung hydatid cyst. Pediatric Infectious Disease Journal 24, 270–272.CrossRefGoogle ScholarPubMed
Bacciarini, L.N., Gottstein, B., Pagan, O., Rehmann, P. & Grone, A. (2004) Hepatic alveolar echinococcosis in cynomolgus monkeys. Veterinary Pathology 41, 229–234.CrossRefGoogle ScholarPubMed
Baz, A., Richieri, A., Puglia, A., Nieto, A. & Dematteis, S. (1999) Antibody response in CD4+ depleted mice after immunization with E. granulosus. Parasite Immunology 21, 141–150.CrossRefGoogle Scholar
Beutler, B. & Cerami, A. (1986) Cachectin/tumor necrosis factor: an endogenous mediator of shock and inflammation. Immunologic Research 5, 281–293.CrossRefGoogle ScholarPubMed
Burton, S.A., Honor, D.J., Mackenzie, A.L., Eckersall, P.D., Markham, R.J.F. & Horney, B.S. (1994) C-reactive protein concentration in dogs with inflammatory leukograms. American Journal of Veterinary Research 55, 613–618.Google ScholarPubMed
Ceciliani, F., Ceron, J.J., Eckersall, P.D. & Sauerwein, H. (2012) Acute phase proteins in ruminants. Journal of Proteomics 75, 4207–4231.CrossRefGoogle ScholarPubMed
Ceron, J.J., Eckersall, P.D. & Subiela, S.M. (2005) Acute phase proteins in dogs and cats: current knowledge and future perspectives. Veterinary Clinical Pathology 34, 85–99.CrossRefGoogle ScholarPubMed
Chiou, M.T., Wang, F.I., Chang, P.H., Liu, C.H., Jeng, C.R., Cheng, C.H., Jou, J. & Pang, V.F. (2001) Hydatidosis in a Chapman's zebra. Journal of Veterinary Diagnostic Investigation 13, 534–537.CrossRefGoogle Scholar
Dilda, F., Pisani, L.F., Rahman, M.Md., Modina, S., Tessaro, I., Sartorelli, P., Ceciliani, F. & Lecchi, C. (2012) Distribution of acute phase proteins in the bovine forestomachs and abomasum. Veterinary Journal 192, 101–105.CrossRefGoogle ScholarPubMed
Dinarello, C.A. (1984) IL-1 and the pathogenesis of the acute phase response. New England Journal of Medicine 311, 1413–1418.Google ScholarPubMed
Dionissopoulos, L., Steele, M.A., AlZahal, O., Plaizier, J.C. & McBride, B.W. (2012) A characterization of inflammatory and structural markers within the rumen epithelium during grain-induced ruminal acidosis in lactating dairy cattle. American Journal of Animal and Veterinary Sciences 7, 141–148.Google Scholar
Ebersole, J. & Cappelli, D. (2000) Acute phase reactants in infectious and inflammatory diseases. Periodontology 23, 19–49.CrossRefGoogle Scholar
Eckersall, P.D. (1995) Acute phase proteins as markers of inflammatory lesions. Comparative Haematology International 5, 93–97.CrossRefGoogle Scholar
Eckersall, P.D. (2000) Recent advances and future prospects for the use of acute phase proteins as markers of disease in animals. Revue de Medecine Veterinaire 151, 577–584.Google Scholar
Eckersall, P.D., Lawson, F.P., Bence, L., Waterston, M.M., Lang, T.L., Donachie, W. & Fontaine, M.C. (2007) Acute phase protein response in an experimental model of ovine caseous lymphadenitis. BMC Veterinary Research 3, 1–6.CrossRefGoogle Scholar
Finkelman, F.D., Pearce, E.J., Urban, J.F. & Sher, A. Jr (1991) Regulation and biological function of helminth-induced cytokine responses. Immunology Today 12, 62–66.CrossRefGoogle ScholarPubMed
Ganheim, C., Hulten, C., Carlsson, U., Kindahl, H., Niskanen, R. & Waller, K.P. (2003) The acute phase response in calves experimentally infected with bovine viral diarrhoea virus and/or Mannheimia haemolytica. Journal of Veterinary Medicine Series B - Infectious Diseases and Veterinary Public Health 50, 183–190.CrossRefGoogle ScholarPubMed
Ganheim, C., Hoglund, J. & Waller, K.P. (2004) Acute phase proteins in response to Dictyocaulus viviparus infection in calves. Acta Veterinaria Scandinavica 45, 79–86.CrossRefGoogle ScholarPubMed
Ghasemi, F., Gonzalez-Cano, P., Griebel, P.J. & Palmer, C. (2012) Proinflammatory cytokine gene expression in endometrial cytobrush samples harvested from cows with and without subclinical endometritis. Theriogenology 78, 1538–1547.CrossRefGoogle ScholarPubMed
Glass, E.J., Craigmie, S.C., Springbett, A., Preston, P.M., Kirvar, E., Wilkie, G.M., Eckersall, P.D., Hall, F.R. & Brown, C.G. (2003) The protozoan parasite, Theileria annulata, induces a distinct acute phase protein response in cattle that is associated with pathology. International Journal for Parasitology 33, 1409–1418.CrossRefGoogle ScholarPubMed
Gronlund, U., Hulten, C., Eckersall, P.D., Hogarth, C. & Waller, K.P. (2003) Haptoglobin and serum amyloid A in milk and serum during acute and chronic experimentally induced Staphylococcus aureus mastitis. Journal of Dairy Research 70, 379–386.CrossRefGoogle ScholarPubMed
Gruys, E., Obwolo, M.J. & Toussaint, M.J.M. (1994) Diagnostic significance of the major acute phase proteins in veterinary clinical chemistry: a review. Veterinary Bulletin 64, 1009–1018.Google Scholar
Haniloo, A., Ghasemi, F., Shikhi, A.K. & Ghavami, M.B. (2008) Immunoregulatory cytokine (TGF-β and IL-10) responses in mice inoculated with protoscoleces and major hydatid fluid antigens of cystic echinococcosis. Iranian Journal of Parasitology 3, 18–23.Google Scholar
Hansen, J. & Perry, B. (1990) The epidemiology, diagnosis and control of gastro-intestinal parasites of ruminants in Africa. Nairobi, English Press Ltd.Google Scholar
Heinrich, P.C., Castell, J.C. & Andus, T. (1990) IL-6 and the acute phase response. Journal of Biochemistry 265, 621–636.CrossRefGoogle ScholarPubMed
Hira, P., Bahr, G., Shweiki, H. & Behbehani, K. (1990) An enzyme linked immunosorbent assay using an arc 5 antigen for the diagnosis of cystic hydatid diseases. Annals of Tropical Medicine and Parasitology 84, 157–162.CrossRefGoogle Scholar
Hofner, M.C., Fosbery, M.W., Eckersall, P.D. & Donaldson, A.I. (1994) Haptoglobin response of cattle infected with foot and mouth disease virus. Research of Veterinary Science 57, 125–128.CrossRefGoogle ScholarPubMed
Holt, J.G., Krieg, N.R., Sneath, P.H.A., Staley, J.T. & Williams, S.T. (2000) Bergey's manual of determinative bacteriology. Philadelphia, Lippincott Williams and Wilkins.Google Scholar
Horadagoda, N.U., Knox, K.M.G., Gibbs, H.A., Reid, S.W.J., Horadagoda, A., Edwards, S.E.R. & Eckersall, P.D. (1999) Acute phase proteins in cattle: discrimination between acute and chronic inflammation. Veterinary Record 144, 437–441.CrossRefGoogle ScholarPubMed
Jungerson, G., Jensen, L., Riber, U., Heegard, P.M.H., Petersen, E., Poulsen, J.S.D., Billehansen, V. & Lind, P. (1999) Pathogenecity of selected Toxoplasma gondii isolates in young pigs. International Journal for Parasitology 29, 1307–1319.CrossRefGoogle Scholar
Kushner, I. & Mackiewicz, A. (1993) The acute phase response: an overview. pp. 3–19in Mackiewicz, A., Kushner, I. & Baumann, H. (Eds) Acute phase proteins: Molecular biology, biochemistry and clinical applications. London, CRC Press.Google Scholar
Landman, W.J.M., Gruys, E. & Bwars, R.M. (1994) A syndrome associated with growth depression and amyloid arthropathy in layers: a preliminary report. Avian Pathology 23, 461–470.CrossRefGoogle ScholarPubMed
Maden, M., Ozturk, A.S., Bulbul, A., Avci, G.E. & Yazar, E. (2012) Acute-phase proteins, oxidative stress, and enzyme activities of blood serum and peritoneal fluid in cattle with abomasal displacement. Journal of Veterinary Internal Medicine 26, 1470–1475.CrossRefGoogle ScholarPubMed
Matijatko, V., Mrljak, V., Kıs, I., Kucer, N., Forsek, J., Zivicnjak, T., Romic, Z., Simec, Z. & Ceron, J.J. (2007) Evidence of acute phase response in dogs naturally infected with Babesia canis. Veterinary Parasitology 144, 242–250.CrossRefGoogle ScholarPubMed
Moro, P. & Schantz, P.M. (2009) Echinococcosis: a review. International Journal of Infectious Diseases 13, 125–133.CrossRefGoogle ScholarPubMed
Mosmann, T.R. & Sad, S. (1996) The expanding universe of T-cell subsets: Th1, Th2 and more. Immunology Today 17, 138–146.CrossRefGoogle ScholarPubMed
Nielsen, B.H., Jacobsen, S., Andersen, P.H., Niewold, T.A. & Heegaard, P.M. (2004) Acute phase protein concentrations in serum and milk from healthy cows, cows with clinical mastitis and cows with extramammary inflammatory conditions. Veterinary Record 154, 361–365.CrossRefGoogle ScholarPubMed
Paredes, R., Godoy, P., Rodriguez, B., Garcia, M.P., Cabezón, C., Cabrera, G., Jiménez, V., Hellman, U., Sáenz, L., Ferreira, A. & Galanti, N. (2011) Bovine (Bos taurus) humoral immune response against Echinococcus granulosus and hydatid cyst infertility. Journal of Cellular Biochemistry 112, 189–199.CrossRefGoogle ScholarPubMed
Petersen, H.H., Nielsen, J.P. & Heegard, P.M.H. (2004) Application of acute phase proteins in veterinary clinical chemistry. Veterinary Research 35, 163–187.CrossRefGoogle ScholarPubMed
Price, J.C. & Sheldon, I.M. (2013) Granulosa cells from emerged antral follicles of the bovine ovary initiate inflammation in response to bacterial pathogen-associated molecular patterns via toll-like receptor pathways. Biology of Reproduction 89, 119.CrossRefGoogle ScholarPubMed
Quinn, P.J., Markey, B.K., Carter, M.E., Donnelly, W.J. & Leonard, F.C. (2002) Veterinary microbiology and microbial disease. Iowa, Blackwell Publishing Professional.Google Scholar
Refik, M., Mehmet, N. & Durmaz, R. (2005) Postoperative changes in serum cytokines profile and nitric oxide levels in patients with cystic echinococcosis. Parasite 12, 265–269.CrossRefGoogle ScholarPubMed
Riganò, R., Profumo, E., Teggi, A. & Siracusano, A. (1996) Production of IL-5 and IL-6 by peripheral blood mononuclear cells from patients with Echinococcus granulosus infection. Clinical and Experimental Immunology 105, 456–459.CrossRefGoogle ScholarPubMed
Riganò, R., Profumo, E. & Siracusano, A. (1997) New perspectives in the immunology of Echinococcus granulosus infection. Parassitologia 39, 275–277.Google ScholarPubMed
Riley, E.M., Dixon, J.B., Jenkins, P. & Ross, G. (1986) Echinococcus granulosus infection in mice: host responses during primary and secondary infection. Parasitology 92, 391–403.CrossRefGoogle ScholarPubMed
Sakamoto, T. & Cabrera, P.A. (2003) Immunohistochemical observations on cellular response in unilocular hydatid lesions and lymph nodes of cattle. Acta Tropica 85, 271–279.CrossRefGoogle ScholarPubMed
Salonen, M., Hirvonen, J., Pyorala, S., Sankari, S. & Sandholm, M. (1996) Quantitative determination of bovine serum haptoglobin in experimentally induced E. coli mastitis. Research in Veterinary Science 60, 88–91.CrossRefGoogle Scholar
Sevimli, A., Misirlioğlu, D., Polat, U., Yalçın, M., Akkoç, A. & Uğuz, C. (2005) The effects of vitamin A, pentoxyfylline and methylprednisolone on experimentally induced amyloid arthropathy in brown layer chicks. Avian Pathology 34, 143–149.CrossRefGoogle ScholarPubMed
Sevimli, A., Misirlioğlu, D., Yağcı, A., Bülbül, A., Yilmaztepe, A. & Altunbaş, K. (2008) The role of chicken IL-1β, IL-6 and TNF-α in the occurrence of amyloid arthropathy. Veterinary Research Communications 32, 499–508.CrossRefGoogle ScholarPubMed
Skinner, J.G. & Roberts, L. (1994) Haptoglobin as an indicator of infection in sheep. Veterinary Record 134, 33–36.CrossRefGoogle ScholarPubMed
Solter, P.F., Hoffmann, W.E., Hungerford, L.L., Siegel, J.P., St. Denis, S.H. & Dorner, J.L. (1991) Haptoglobin and ceruloplasmin as determinants of inflammation in dogs. American Journal of Veterinary Research 52, 1738–1742.Google Scholar
Soulsby, E.J.L. (1982) Helminths, arthropods and protozoa of domesticated animals. 7th edn.London, Baillière Tindal.Google Scholar
Thompson, R.C.A. (1995) Biology and systematics of Echinococcus. pp. 1–50in Thompson, R.C.A. & Lymbery, A.J. (Eds) Echinococcus and hydatid disease. Wallingford, UK, CAB International.Google Scholar
Tliba, O., Sibille, P., Boulard, C. & Chauvin, A. (2002) Early hepatic cytokine mRNA expression in experimental rat fasciolosis. Veterinary Parasitology 103, 237–249.CrossRefGoogle ScholarPubMed
Trevisi, E., Amadori, M., Cogrossi, S., Razzuoli, E. & Bertoni, G. (2012) Metabolic stress and inflammatory response in high-yielding, periparturient dairy cows. Research in Veterinary Science 93, 695–704.CrossRefGoogle ScholarPubMed
Turgay, N. & Üstün, Ş. (2004) Echinococcosisde immun cevap. pp. 107–113in Altıntaş, N., Tınar, R. & Çoker, A. (Eds) Echinococcosis. İzmir, Ege Üniversitesi Matbaası.Google Scholar
Ulutaş, P.A., Voyvoda, H., Ulutaş, B. & Aypak, S. (2008) Miks helmint enfeksiyonlu keçilerde haptoglobin, SAA ve seruloplazmin konsantrasyonları. Turkiye Parazitoloji Dergisi 32, 229–233.Google Scholar
Urquhart, G.M., Armour, J., Duncan, J., Dunn, A.M. & Jennings, F.W. (1987) Veterinary parasitology. pp. 271–272. London, Longman Scientific and Technical.Google Scholar
Weidmeyer, C.E. & Solter, P.F. (1996) Validation of human haptoglobin immunoturbidimetric assay for detection of haptoglobin in equine and canine serum and plasma. Veterinary Clinical Pathology 25, 141–146.CrossRefGoogle ScholarPubMed
Ziino, G., Giuffrida, A., Bilei, S. & Panebianco, A. (2009) Bacteria isolated from 25 hydatid cysts in sheep, cattle and goats. Veterinary Record 165, 234–236.CrossRefGoogle ScholarPubMed