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Research (Published online: 14-12-2016)

13. Evidence of hemolysis in pigs infected with highly virulent African swine fever virus - Zaven Karalyan, Hovakim Zakaryan, Elina Arakelova, Violeta Aivazyan, Marina Tatoyan, Armen Kotsinyan, Roza Izmailyan and Elena Karalova

Veterinary World, 9(12): 1413-1419

 

 

   doi: 10.14202/vetworld.2016.1413-1419

 

Zaven Karalyan: Laboratory of Cell Biology and Virology, Institute of Molecular Biology of NAS RA, 7 Hasratyan Street, 0014 Yerevan, Armenia; zkaralyan@yahoo.com

Hovakim Zakaryan: Laboratory of Cell Biology and Virology, Institute of Molecular Biology of NAS RA, 7 Hasratyan Street, 0014 Yerevan, Armenia; hovakimzakaryan@gmail.com

Elina Arakelova: Laboratory of Human Genomics and Immunomics, Institute of Molecular Biology of NAS RA, 7 Hasratyan Street, 0014 Yerevan, Armenia; elinaa72@mail.ru

Violeta Aivazyan: Laboratory of Human Genomics and Immunomics, Institute of Molecular Biology of NAS RA, 7 Hasratyan Street, 0014 Yerevan, Armenia; viola_ay@yahoo.com

Marina Tatoyan: Laboratory of Cell Biology and Virology, Institute of Molecular Biology of NAS RA, 7 Hasratyan Street, 0014 Yerevan, Armenia; marina.tatoyan@mail.ru

Armen Kotsinyan: Laboratory of Cell Biology and Virology, Institute of Molecular Biology of NAS RA, 7 Hasratyan Street, 0014 Yerevan, Armenia; armenrkotsinyan@gmail.com

Roza Izmailyan: Laboratory of Cell Biology and Virology, Institute of Molecular Biology of NAS RA, 7 Hasratyan Street, 0014 Yerevan, Armenia; izmruzanna@gmail.com

Elena Karalova: Laboratory of Cell Biology and Virology, Institute of Molecular Biology of NAS RA, 7 Hasratyan Street, 0014 Yerevan, Armenia; z_karalyan@mb.sci.am

 

Received: 29-08-2016, Accepted: 12-11-2016, Published online: 14-12-2016

 

Corresponding author: Zaven Karalyan, e-mail: zkaralyan@yahoo.com


Citation: Karalyan Z, Zakaryan H, Arakelova E, Aivazyan V, Tatoyan M, Kotsinyan A, Izmailyan R, Karalova E (2016) Evidence of hemolysis in pigs infected with highly virulent African swine fever virus, Veterinary World, 9(12): 1413-1419.



Aim: The research was conducted to understand more profoundly the pathogenetic aspects of the acute form of the African swine fever (ASF).

Materials and Methods: A total of 10 pigs were inoculated with ASF virus (ASFV) (genotype II) in the study of the red blood cells (RBCs), blood and urine biochemistry in the dynamics of disease.

Results: The major hematological differences observed in ASFV infected pigs were that the mean corpuscular volume, mean corpuscular hemoglobin, and hematocrits were significantly decreased compared to controls, and the levels of erythropoietin were significantly increased. Also were detected the trends of decrease in RBC count at terminal stages of ASF. Analysis of blood biochemistry revealed that during ASF development, besides bilirubinemia significantly elevated levels of lactate dehydrogenase, and aspartate aminotransferase were detected. Analysis of urine biochemistry revealed the presence of bilirubinuria, proteinuria during ASF development. Proteinuria, especially at late stages of the disease reflects a severe kidney damage possible glomerulonefritis.

Conclusion: The results of this study indicate the characteristics of developing hemolytic anemia observed in acute ASF (genotype II).

Keywords: African swine fever virus, bilirubinemia, bilirubinuria, erythropoietin, hemolysis, proteinuria.



1. Oura, C. (2013) African swine fever virus: On the move and dangerous. Vet. Rec., 173: 243-245.
https://doi.org/10.1136/vr.f5327
PMid:24038277
 
2. Blome, S., Gabriel, C. and Beer, M. (2013) Pathogenesis of African swine fever in domestic pigs and European wild boar. Virus Res., 173: 122-130.
https://doi.org/10.1016/j.virusres.2012.10.026
PMid:23137735
 
3. Mu-oz, A., Riber, C., Trigo, P. and Castejón, F. (2012) Age-and gender-related variations in hematology, clinical biochemistry, and hormones in Spanish fillies and colts. Res. Vet. Sci., 93: 943-949.
https://doi.org/10.1016/j.rvsc.2011.11.009
PMid:22230595
 
4. Rowlands, R.J., Michaud, V., Heath, L., Hutchings, G., Oura, C., Vosloo, W., Dwarka, R., Onashvili, T., Albina, E. and Dixon, L.K. (2008) African swine fever virus isolate, Georgia. Emerg. Infect. Dis., 14: 1870-1874.
https://doi.org/10.3201/eid1412.080591
PMid:19046509 PMCid:PMC2634662
 
5. Enjuanes, L., Carrascosa, A.L., Moreno, M.A. and Vi-uela, E. (1976) Titration of African swine fever (ASF) virus. J. Gen. Virol., 32: 471-477.
https://doi.org/10.1099/0022-1317-32-3-471
PMid:823294
 
6. Bacus, J.W. (1980) Quantitative morphological analysis of red blood cells. Blood Cells, 6: 295-314.
PMid:7397389
 
7. Bacus, J.W. (1984) Quantitative red cell morphology. Monogr. Clin. Cytol., 9: l-27.
https://doi.org/10.1159/000409900
 
8. Hanion-Lundberg, K.M., Kirby, R.S., Gandhi, S. and Broekhuizen, F.F. (1997) Nucleated red blood cells in cord blood of singleton term neonates. Am. J. Obstet. Gynecol., 176: 1149-1154.
https://doi.org/10.1016/S0002-9378(97)70328-4
 
9. Gomez-Villamandos, J.C., Bautista, M.J., Carrasco, L., Caballero, M.J., Hervas, J., Villeda, C.J., Wilkinson, P.J. and Sierra, M.A. (1997) African swine fever virus infection of bone marrow: Lesions and pathogenesis. Vet. Pathol., 34: 97-107.
https://doi.org/10.1177/030098589703400202
 
10. Karalyan, Z., Zakaryan, H., Arzumanyan, H., Sargsyan, K., Voskanyan, H., Hakobyan, L., Abroyan, L., Avetisyan, A. and Karalova, E. (2012) Pathology of porcine peripheral white blood cells during infection with African swine fever virus. BMC Vet. Res., 8: 18.
https://doi.org/10.1186/1746-6148-8-18
PMid:22373449 PMCid:PMC3308919
 
11. Gómez-Villamandos, J.C., Bautista, M.J., Sánchez-Cordón, P.J. and Carrasco, L. (2013) Pathology of African swine fever: The role of monocyte-macrophage. Virus Res., 173: 140-149.
https://doi.org/10.1016/j.virusres.2013.01.017
PMid:23376310
 
12. Howey, E.B., O'Donnell, V., de Carvalho Ferreira, H.C., Borca, M.V. and Arzt, J. (2013) Pathogenesis of highly virulent African swine fever virus in domestic pigs exposed via intraoropharyngeal, intranasopharyngeal, and intramuscular inoculation, and by direct contact with infected pigs. Virus Res., 178: 328-339.
https://doi.org/10.1016/j.virusres.2013.09.024
PMid:24076499
 
13. Hervás, J., Gómez-Villamandos, J.C., Méndez, A., Carrasco, L. and Sierra, M.A. (1996) The lesional changes and pathogenesis in the kidney in African swine fever. Vet. Res. Commun., 20: 285-299.
https://doi.org/10.1007/BF00366926
PMid:8739527
 
14. Okpara, R.A. (1985) Normoblasts in peripheral blood of Nigerians: Their clinical significance. J. Natl. Med. Assoc., 77: 899-903.
PMid:4078915 PMCid:PMC2571209
 
15. Tavassoli, M. (1975) Erythroblastemia. West. J. Med., 122: 194-198.
PMid:1096474 PMCid:PMC1129678
 
16. Harvey, J.W. (2001) Atlas of Veterinary Hematology: Blood and Bone Marrow of Domestic Animals. W. O. Saunders Company, Philadelphia, PA. p224.
 
17. Evans, E.R. (1951) Diagnosis of the hemolytic anemias. Calif. Med., 75: 271-275.
PMid:14879272 PMCid:PMC1520966
 
18. De Klerk, G., Rosengarten, P.C., Vet, R.J. and Goudsmit, R. (1981) Serum erythropoietin (EST) titers in anemia. Blood, 58: 1164-1170.
PMid:7306704
 
19. Richmond, T.D., Chohan, M. and Barber, D.L. (2005) Turning cells red: Signal transduction mediated by erythropoietin. Trends Cell. Biol., 15: 146-155.
https://doi.org/10.1016/j.tcb.2005.01.007
PMid:15752978
 
20. Tada, K. and Watanabe, Y. (1962) Serum enzymes in experimental hemolysis: Aldolase, glucose-6-phosphate dehydrogenase and lactic dehydrogenase in serum of rabbits with acute hemolysis by acetylphenylhydrazine. Tohoku J. Exp. Med., 75: 397-402.
https://doi.org/10.1620/tjem.75.397
 
21. Kato, G.J., McGowan, V., Machado, R.F., Little, J.A., Taylor, J.6th, Morris, C.R., Nichols, J.C., Wang, X., Poljakovic, M., Morris, S.M.Jr. and Gladwin, M.T. (2006) Lactate dehydrogenase as a biomarker of hemolysis-associated nitric oxide resistance, priapism, leg ulceration, pulmonary hypertension, and death in patients with sickle cell disease. Blood, 107: 2279-2285.
https://doi.org/10.1182/blood-2005-06-2373
PMid:16291595 PMCid:PMC1895723
 
22. Dunkan, J.R. and Prasse, K.W. (1979) Veterinary Laboratory Medicine. The Iowa State University Press, Ames. p82.
 
23. Hess, C.E., Ayers, C.R., Wetzel, R.A., Mohler, D.N. and Sandusky, W.R. (1971) Dilutional anemia of splenomegaly: An indication for splenectomy. Ann. Surg., 173: 693-699.
https://doi.org/10.1097/00000658-197105000-00009
 
24. Wang, Z., Vogel, O., Kuhn, G., Gassmann, M. and Vogel, J. (2013) Decreased stability of erythroblastic islands in integrin ß3-deficient mice. Physiol. Rep., 1(2): e00018.
https://doi.org/10.1002/phy2.18
PMid:24303107 PMCid:PMC3831914
 
25. Emilia, G., Luppi, M., Ferrari, M.G., Barozzi, P., Marasca, R. and Torelli, G. (1997) Hepatitis C virus-induced leuko-thrombocytopenia and haemolysis. J. Med. Virol., 53: 182-184.
https://doi.org/10.1002/(SICI)1096-9071(19971003)53:2<182::AID-JMV12>3.0.CO;2-L
 
26. Herry, I., Cadranel, J., Antoine, M., Meharzi, J., Michelson, S., Parrot, A., Rozenbaum, W. and Mayaud, C. (1996) Cytomegalovirus-induced alveolar hemorrhage in patients with AIDS: A new clinical entity? Clin. Infect. Dis., 22: 616-620.
https://doi.org/10.1093/clinids/22.4.616
PMid:8729198
 
27. Cammack, N. and Gould, E.A. (1985) Conditions for haemolysis by flaviviruses and characterization of the haemolysin. J. Gen. Virol., 66: 2291-2296.
https://doi.org/10.1099/0022-1317-66-10-2291
PMid:2995565
 
28. Adu, F., Esan, J. and Baba, S.S. (1990) Seroepidemiological survey for yellow fever antibodies in domestic animals. Rev. Roum. Virol., 41: 147-150.
PMid:2099827
 
29. Hod, E.A., Zimring, J.C. and Spitalnik, S.L. (2008) Lessons learned from mouse models of hemolytic transfusion reactions. Curr. Opin. Hematol., 15: 601-605.
https://doi.org/10.1097/MOH.0b013e328311f40a
PMid:18832931 PMCid:PMC2646405
 
30. Xu, W.S., Qiu, X.M., Ou, Q.S., Liu, C., Lin, J.P., Chen, H.J., Lin, S., Wang, W.H., Lin, S.R. and Chen, J. (2015) Red blood cell distribution width levels correlate with liver fibrosis and inflammation: A noninvasive serum marker panel to predict the severity of fibrosis and inflammation in patients with hepatitis B. Medicine (Baltimore), 94: e612.
https://doi.org/10.1097/md.0000000000000612
 
31. Sornjai, W., Khungwanmaythawee, K., Svasti, S., Fucharoen, S., Wintachai, P., Yoksan, S., Ubol, S., Wikan, N. and Smith, D.R. (2014) Dengue virus infection of erythroid precursor cells is modulated by both thalassemia trait status and virus adaptation. Virology, 471-473: 61-71.
https://doi.org/10.1016/j.virol.2014.10.004
PMid:25461532
 
32. Breese, S.S.Jr. and Hess, W.R. (1966) Electron microscopy of African swine fever virus hemadsorption. J. Bacteriol., 92: 272-274.
PMid:5949565 PMCid:PMC276226
 
33. Karalova, E.M., Voskanian, G.E., Sarkisian, K.H.V., Abroian, L.O., Avetisian, A.S., Akopian, L.A., Semerdzhian, Z.B., Zakarian, O.S., Arzumanian, G.A. and Karalian, Z.A. (2011) Pathology of lymphoid tissue cells infected by African swine fever virus in vitro. Vopr. Virusol., 56: 33-37.
PMid:21427953
 
34. Zakaryan, H., Cholakyans, V., Simonyan, L., Misakyan, A., Karalova, E., Chavushyan, A. and Karalyan, Z. (2015) A study of lymphoid organs and serum proinflammatory cytokines in pigs infected with African swine fever virus genotype II. Arch. Virol., 160: 1407-1414.
https://doi.org/10.1007/s00705-015-2401-7
PMid:25797197
 
35. Jelkmann, W. (1998) Proinflammatory cytokines lowering erythropoietin production. J. Interferon. Cytokine. Res., 18: 555-559.
https://doi.org/10.1089/jir.1998.18.555
PMid:9726435
 
36. Wang, T., Tu, M.F., Zhu, J., Zheng, W. and Shao, Z.H. (2013) The role of cytokines in lymphoma with anemia. Zhongguo Shi Yan Xue Ye Xue Za Zhi., 21: 392-395.
PMid:23628039
 
37. Gómez-Villamandos, J.C., Hervás, J., Méndez, A., Carrasco, L., Martín de las Mulas, J., Villeda, C.J., Wilkinson, P.J. and Sierra, M.A. (1995) Experimental African swine fever: Apoptosis of lymphocytes and virus replication in other cells. J. Gen. Virol., 76: 2399-2405.
https://doi.org/10.1099/0022-1317-76-9-2399