Determination of Malondialdehyde, Nitric Oxide, Reduced Glutathione, Sialic Acid and Ceruloplasmin Levels in Sheep Liver Tissue With Hydatic Cyst

Abstract

Cystic echinococcosis is a prevalent helminth-zoonosis that poses a significant threat to human and animal health worldwide. Although it typically shows an asymptomatic clinical course, it has been reported to cause many damages and biochemical changes in tissues and organism. The aim of this study was to investigate the concentrations of nitric oxide (NO), reduced glutathione (GSH), malondialdehyde (MDA), ceruloplasmin (Cp), and total sialic acid (TSA) in sheep liver tissue affected by cystic echinococcosis. The study was carried out on sheep between 4-5 years of age brought to the slaughterhouse in the Igdir territory. The livers were examined post-mortem for cystic echinococcosis and cystic structures. Sheep liver tissues that tested positive for protoscolex were designated as the ‘infected group’, while healthy sheep liver tissues without lesions were assigned to the ‘control group’. The results showed significantly higher levels of NO, MDA, Cp and TSA in the infected group compared to the control group (p<0.05), while GSH levels were significantly lower (p<0.05). These findings indicate that cystic echinococcosis in sheep is closely associated with mechanisms of inflammation, oxidative stress, and tissue damage. Moreover, our study provides insights into the oxidative response of cystic echinococcosis in liver tissue and enhances our understanding of the disease’s pathogenesis.

Keywords

• Cystic Echinococcosis
• Sheep
• Inflammation
• Oxidative Stress

Hidatik Kistli Koyun Karaciğer Dokusunda Malondialdehit, Nitrik Oksit, İndirgenmiş Glutatyon, Sialik Asit ve Seruloplazmin Düzeylerinin Belirlenmesi

Öz

Kistik ekinokokkoz, dünya çapında insan ve hayvan sağlığına ciddi bir tehdit oluşturan yaygın bir helmint-zoonozdur. Genellikle semptomsuz bir klinik seyir göstermesine rağmen, birçok doku ve organizmada hasara ve biyokimyasal değişikliklere neden olduğu bildirilmiştir. Bu çalışmanın amacı, kistik ekinokokkoz etkisi altındaki koyun karaciğer dokusunda nitrik oksit (NO), indirgenmiş glutatyon (GSH), malondialdehit (MDA), seruloplazmin (Cp) ve toplam sialik asit (TSA) konsantrasyonlarını araştırmaktı. Çalışma, Iğdır bölgesinde kesimhaneye getirilen 4-5 yaş arası koyunlar üzerinde gerçekleştirildi. Karaciğerler, ölümden sonra kistik ekinokokkoz ve kistik yapılar için incelendi. Protoskol eksisi pozitif çıkan koyun karaciğer dokuları "enfekte grubu" olarak adlandırıldı, lezyon olmayan sağlıklı koyun karaciğer dokuları ise "kontrol grubu" olarak atanmıştır. Sonuçlar, enfekte grubun NO, MDA, Cp ve TSA seviyelerinin kontrol grubuna göre önemli ölçüde yüksek olduğunu gösterdi (p<0.05), buna karşın GSH seviyelerinin önemli ölçüde düşük olduğunu ortaya koydu (p<0.05). Bu bulgular, kistik ekinokokkozun koyunlarda iltihaplanma, oksidatif stres ve doku hasarı mekanizmalarıyla yakından ilişkili olduğunu göstermektedir. Ayrıca, çalışmamız kistik ekinokokkozun karaciğer dokusundaki oksidatif yanıtını anlamamıza ve hastalığın patogenezi hakkındaki anlayışımızı artırmamıza yardımcı olmaktadır.

Anahtar Kelimeler

• İnflamasyon
• Kistik Ekinokokkozis
• Oksidatif Stres
• Koyun

References

1. Aslam, H., Bi, S., Irshadullah, M. (2023). Analysis of antioxidant enzymes and oxidative stress markers in the liver of naturally infected Indian water buffalo (Bubalus bubalis) with cystic echinococcosis. Journal of Parasitic Diseases, 1-9. 47(2):340–348. https://doi.org/10.1007/s12639-023-01578-7
2. Ayaz, E., Ertekin, A., Ozdal, N., Tas, Z. (2006). Some Biochemical Parameters in Sheep Infected with Endoparasites (Fasciola spp. Dicrocoelium dendriticum, Hydatid cysts, Trichostrongylidae and Protostrongylidae). Turkiye Parazitol Derg, 30(4), 57-61.
3. Beutler, E., Duron, O., Kelly, B.M. (1963). Improved method for determination of blood glutathione. Journal of Laboratory and Clinical Medicine. 61, 882-888.
4. Boczon, K., Hadas, E., Wandurska-Nowak, E., Derda, M. (1996). A stimulation of antioxidants in muscles of Trichinella spiralis infected rats. Acta Parasitologica, 3(41).
5. Bozukluhan, K., Merhan, O., Gökçe, H. İ., Metin, Ö., Atakişi, E., Kızıltepe, Ş., Gökçe, G. (2018). Determination of some acute phase proteins, biochemical parameters and oxidative stress in sheep with naturally infected sheeppox virus. Kafkas Üniversitesi Veteriner Fakültesi Dergisi, 24(3),437-441. DOI : 10.9775/kvfd.2017.19167
6. Bozukluhan, K., Merhan, O., Kızıltepe, Ş., Harmankaya, A., Gökçe, G. (2020). Determination of oxidative stress and ceruloplasmin levels in sheep with toxoplasmosis. Van Veterinary Journal, 31(2). https://doi.org/10.36483/vanvetj.646976
7. Colombo, J., Richterich R. (1964). Zur Bestimmung Des ceruloplasmin in plasma. Schweiz Med Wschr, 94, 715-720.
8. Craigi, P.S., Mc. Manus, D.P., Lightowlers, M.W. et al. (2007). Prevention and control of cystic echinococcosis. Lancet Infect Disease, 7, 385-394. doi: 10.1016/S1473-3099(07)70134-2.

9. Dede, S., Değer, Y., Değer, S., Alkan, M. (2000). Bazı endoparazitlerle (Fasciola sp. + Trichostrongylidae sp. + Eimeria sp.) enfekte koyunlarda lipit peroksidasyonu ve antioksidan durumunun saptanması. Türkiye Parazitol Dergisi, 24(1), 190-193.
10. Deger, Y., Ertekin, A., Deger, S., Mert, H. (2008). Lipid peroxidation and antioxidant potential of sheep liver infected naturally with distomatosis. Turkiye Parazitol Derg, 32, 23–26.
11. Değer, S., Değer, Y., Ertekin, A., Gül, A., Biçek, K., Özdal, N. (2008). Dictyocaulus viviparus ile enfekte sığırlarda lipit peroksidasyon ve antioksidan durumunun saptanması. Türkiye Parazitol Dergisi, 32(3), 234-237.
12. Demir, P., Mor, N. (2011). Kars Belediye Mezbahasında Kesilen Sığırlarda Kistik Echinococcosis’ in Yaygınlığı, Mevsimsel Dağılımı ve Ekonomik Önemi. Turkiye Parazitol Dergisi, 35, 185-188.
13. Derda, M., Wandurska-Nowak, E., Hadas, E. (2004). Changes in the level of antioxidants in the blood from mice infected with Trichinella spiralis. Parasitol. Research, 93, 207–210. DOI 10.1007/s00436-004-1093-9
14. Dimri, U., Sharma, M.C. Yamdagni, A., Ranjan, R., Zama, M. M. S. (2010). Psoroptic mange infestation increases oxidative stress and decreases antioxidant status in sheep. Veterinary Parasitology, 168, 318–322. https://doi.org/10.1016/j.vetpar.2009.11.013
15. Erdogan, H. M., Karapehlivan, M., Citil, M., Atakisi, O., Uzlu, E., Unver, A. (2008). Serum sialic acid and oxidative stress parameters changes in cattle with leptospirosis. Veterinary Research Communications, 32, 333-339. DOI 10.1007/s11259-008-9036-z
16. Erkılıç, E., Merhan, O., Kirmizigul, A., Ogun, M., Akyuz, E., Citil, M. (2019). Salivary and serum levels of serum amyloid a, haptoglobin, ceruloplasmin and albumin in neonatal calves with diarrhoea. Kafkas Universitesi Veteriner Fakultesi Dergisi, 25(4). DOI: 10.9775/kvfd.2018.21424
17. Ersayit, D., Kilic, E., Yazar, S., Artis, T. (2009). Oxidative stress in patients with cystic echinococcosis: relationship between oxidant and antioxidant parameters. Saglık Bilimleri Dergisi, 18, 159-166.
18. Eser, İ., Ulaş, T., Kürkçüoğlu, İ. C., Aydoğan, H., Sak, Z. H. A., Aydın, M. S, Aksoy, N. at al. (2013). Evaluation of ceruloplasmin levels in patients with pulmonary cystic echinococcus. Clin Ter, 164(2), e89-92. doi: 10.7417/CT.2013.1537. doi: 10.7417/CT.2013.1537
19. Fang, Y.Z., Yang, S., Wu, G. (2002). Free radicals, antioxidants, and nutrition. Nutrition, 18, 872–879. https://doi.org/10.1016/s0899-9007(02)00916-4
20. Floris, G., Medda, R., Padiglia, A., Musci, G. (2000). The physiopathological significance of ceruloplasmin: a possible therapeutic approach. Biochem Pharmacol, 60(12), 1735-1741. https://doi.org/10.1016/S0006-2952(00)00399-3
21. Gabrashanska, M., Teodorova, S.E., Anisimova, M. (2008). Oxidative-antioxidant status of Fasciola hepatica-infected rats supplemented with zinc. A mathematical model for zinc bioaccumulation and host growth. Parasitol Research, 104, 69–78. DOI 10.1007/s00436-008-1160-8
22. Gıcık, Y., Arslan, M. Ö., Kara, M., Köse, M. (2004). Kars ilinde kesilen sığır ve koyunlarda kistik ekinokokkozisin yaygınlığı. Türkiye Parazitoloji Dergisi, 28(3), 136-139.
23. Gökce, H. İ., Bozukluhan, K., (2009). Çiftlik hayvanlarında önemli akut faz proteinleri ve bunların veteriner hekimlik alanındaki kullanımı. Dicle Üniversitesi Veteriner Fakültesi Dergisi, (1), 1-14.
24. Gruys, E., Oblowo, M.J., Toussaint, J. (1994). Diagnosis significance of major acute phase proteins in veterinary clinical chemistry: A review. Vet Bull, 11, 1009-1015.
25. Heidarpour, M., Mohri, M., Borji, H., Moghadas, E. (2013a). Oxidant/antioxidant balance and trace elements status in sheep with liver cystic echinococcosis. Comparative Clinical Pathology, 22, 1043–1049. DOI 10.1007/s00580-012-1523-5
26. Heidarpour, M., Mohri, M., Borji, H., Moghdass, E. (2012). Oxidative stress and trace elements in camel (Camelus dromedarius) with liver cystic echinococcosis. Veterinary Parasitology, 187, 459–463. doi: 10.1016/j.vetpar.2012.01.015
27. Heidarpour, M., Mohri, M., Borji, H., Moghdass, E. (2013b). Oxidant/antioxidant status in cattle with liver cystic echinococcosis. Vet Parasitol, 195, 131–135. doi: 10.1016/j.vetpar.2013.01.018.
28. Karaman, U., Celik, T., Kiran, T. R., Colak, C., Daldal, N. U., (2008). Malondialdehyde, glutathione, and nitric oxide levels in Toxoplasma gondii seropositive patients. The Korean Journal of Parasitology, 46(4), 293. DOI: 10.3347/kjp.2008.46.4.293
29. Kaya, S., Sutcu, R., Cetin, E.S., Arıdogan, B.C., Delibas, N., Demirci, M. (2007). Lipid peroxidation level and antioxidant enzyme activities in the blood of patients with acute and chronic fascioliasis. International Journal of Infectious Diseases: Home Page, 11, 251–255. DOI: 10.1016/j.ijid.2006.05.003
30. Kilic, E., Yazar, S., Baskol, G., Artis, T., Ersayit, D., (2010). Antioxidant and nitric oxide status in patients diagnosed with Echinococcus granulosus. African Journal of Microbiology Research, 4(22), 2439-2443.
31. Kilic, E., Yazar, S., Saraymen, R., Ozbilge, H. (2003). Serum malondialdehyde level in patients infected with Ascaris lumbricoides. World Journal of Gastroenterology, 9(10), 2332-2334. doi: 10.3748/wjg.v9.i10.2332
32. Kırmızıgül, A. H., Erkılıç, E. E., Merhan, O., Öğün, M., Ölmez, N., Taşçi, G. T., Vatansever, Z. (2020). The serum amyloid-a, haptoglobin, ceruloplasmin and albumin levels in dogs which are infected with Babesia canis. Kocatepe Veterinary Journal, 13(2), 219-223. DOI: 10.30607/kvj.670744
33. Kolodziejczyk, L., Siemieniuk, E., Skrzydlewska, E. (2006). Fasciola hepatica: effects on the antioxidative properties and lipid peroxidation of rat serum. Experimental Parasitology, 113, 43–48. https://doi.org/10.1016/j.exppara.2005.12.005
34. Koltas, I.S., Yucebilgic, G., Biligin, R., Parsak, C.K., Sakman, G. (2006). Serum malondialdehyde level in patients with cystic echinococcosis. Saudi Medical Journal, 27, 1703–1705. PMID: 17106545
35. Latif, A.A., Tanveer, A., Maqbool, A., Siddiqi, N., Kyaw-Tanner, M., Traub, R.J. (2010). Morphological and molecular characterisation of Echinococcus granulosus in livestock and humans in Punjab, Pakistan. Veterinary parasitology, 170(1-2), 44-49. DOI: 10.1016/j.vetpar.2010.02.003
36. Mahmood, E. A. K., Handan, M., Nihat, M. (2020). Determination of Oxidant/Antioxidant Levels in Sheep with Hydatite Cyst in Liver. Indian Journal of Forensic Medicine & Toxicology, 14(2), 1235-1238. https://doi.org/10.37506/ijfmt.v14i2.3075
37. McManus, D.P., Zhang, W., Li, J., Bartley, P.B. (2003). Echinococcosis. Lancet, 362, 1295–1304. DOI: 10.1016/S0140-6736(03)14573-4
38. McPearson, R. (1996). Clinical Diagnosis and Management by Laboratory Methods. In: Henry JB, W.B. Saunders Company Philadelphia, 237-257.
39. Merhan O., Bozukluhan K., Gokce H.I. (2017). Acute phase proteins and biochemical and oxidative stress parameters in Hypoderma spp. infested cattle. Journal of the Hellenic Veterinary Medical Society, 68(4), 535-540. https://doi.org/10.12681/jhvms.16049
40. Mert, N., Kozat, S., Ekin, S., Gunduz, H., Denizhan, V. (2003). Doğal kronik Fasciolasisli koyunlarda serum sialik asit ve serum lipid-bağlı sialik asit düzeyleri. 13. Ulusal Parazitoloji Kongresi, 8-12 Eylül 2003, Konya, Turkey.
41. Miranda, K.M. ,Espey, M.G., Wink, D.A. (2001). A rapid, simple spectrophotometric method for simultaneous detection of nitrate and nitrite. Nitric Oxide, 5(1), 62-71. DOI: 10.1006/niox.2000.0319
42. Mohammadpour, O., Rasouli, S., Azimzadeh, K., Salarpour, M., Narouie, A. (2021). Evaluation of plasma changes of hepcidin, total sialic acid and sphingosine 1 phosphate in buffaloes with hepatic hydatidosis. Journal of Basic and Clinical Veterinary Medicine, 2(1), 32-37.
43. Nakajima, Y., Momotani, E., Murakami, T., Ishikawa, Y., Morimatsu, M., Saito, M., Suzuki, H., Yasukawa, K. (1993). Induction of acute phase protein by recombinant human interleukin-6 (IL-6) in calves. Vet Immunol Immunopathol, 35, 385-391. https://doi.org/10.1016/0165-2427(93)90047-8
44. Nart, D. (2004). Cystic ve alveolar echinococcosis patogenezi. In: Altıntas N, Tınar R, Çoker A. (Eds.), Echinococcosis. Hidatitoloji Dern Yay 1, 149–158.
45. Nisbet, C., Çenesiz, S., Açıcı, M., Umur, Ş. (2008). Kistik ekinokokkozisli sığırlarda serum malondialdehit, seruloplazmin ve adenozin deaminaz düzeylerinin belirlenmesi. Erciyes Üniversitesi Veteriner Fakültesi Dergisi, 5(1), 1-5.
46. Oku, Y., Malgor, R., Benavidez, U., Carmona, C., Kamiya, H. (2004). Control program against hydatidosis and the decreased prevalence in Uruguay. International Congress Series, 1267, 98-104. https://doi.org/10.1016/j.ics.2004.01.087
47. Özcel, A., İnci, A., Turgay, N., Köroğlu, E. (2007). Tıbbi ve Veteriner İmmunoparazitolojisi. Kistik Ekinokokkozis ve İmmunolojisi. Altıntaş N, Yolasığmaz A, Türkiye Parazitoloji derneği yayınları, 259.
48. Rashid S, Irshadullah M (2019). Evaluation of antioxidant and oxidant status of goats (Capra aegagrus hircus) naturally infected with Haemonchus contortus. Journal Helminthology, 94, 36. DOI: https://doi.org/10.1017/S0022149X19000117
49. Rehman, A., Rehman, L., Ullah, R., Beg, M. A., Khan, M. H., Abidi, S. M. A. (2021). Oxidative status and changes in the adenosine deaminase activity in experimental host infected with tropical liver fluke, Fasciola gigantica. Acta Tropica, 213, 105753. https://doi.org/10.1016/j.actatropica.2020.105753
50. Saadi, A., Amarir, F., Filali, H., Thys, S., Rhalem, A., Kirschvink, N., Raes, M., Marcotty, T., Oukessou, M., Duchateau, L., Sahibi, H. (2020). The socio-economic burden of cystic echinococcosis in Morocco: a combination of estimation method. PLoS Negl Trop Dis, 14, e0008410. https://doi.org/10.1371/journal.pntd.0008410
51. Saleh MA. (2008). Circulating oxidative stress status in desert sheep naturally infected with Fasciola hepatica. Veterinary Parasitology, 154, 262–269. https://doi.org/10.1016/j.vetpar.2008.03.012
52. Saleh, M. A., Al-Salahy, M. B., Sanousi, S. A. (2009). Oxidative stress in blood of camels (Camelus dromedaries) naturally infected with Trypanosoma evansi. Veterinary Parasitology, 162, 192–199. https://doi.org/10.1016/j.vetpar.2009.03.035
53. Sanchez-Campos, S., Tunon, M. J., Gonzales, P., Gonzales-Gallego, J. (1999). Oxidative stress and changes in liver antioxidant enzymes induced by experimental dicrocoeliosis in hamsters. Parasitology Research, 85, 468–474.
54. Shousha, S. A., Khalil, S. S., Rashwan, E. A. (1999). Oxygen free radical and nitric oxide production in single or combined human schistosomiasis and fascioliasis. Journal of the Egyptian Society of Parasitology, 29(1).
55. Sydow, G., Wittmann, W., Bender, E., Starick, E. (1988). The sialic acid content of the serum of cattle infected with bovine leukosis virus. Arch Exp Veterinarmed journal articles from PubMed, 42, 194-197.
56. Şahin, T., Akgul, Y. (2006). Investigation of Some Trace Element Levels and Biochemical Parameters in Sheep with Endoparasite. YYÜ Sağlık Bilimleri Dergisi, 9(1), 100-106.
57. Şener, S., Yazar, S., Şahin, İ. (2004). Cystic Echinococcosis'in indirekt fluoresan antikor testi (IFAT) ile tanısında kullanılan antijenlerin tanı değerlerinin araştırılması. Erciyes Üniversitesi Sağlık Bilimleri Dergisi, 13(1), 1-6.
58. Şimşek, S., Yüce, A., Ütük, A. E. (2006). Determination of serum malondialdehyde levels in sheep naturally infected with Dicrocoelium dendriticum. FU Saglık Bil Dergisi, 20(3), 217-220.
59. Tuna, G. E., Ulutaş, B. (2015). Hastalıkların biyobelirteçleri olarak akut faz proteinleri. Türkiye Klinikleri J Vet Sci Intern Med-Special Topics, 1(1), 8-19.
60. Ulutaş, P.A., Voyvoda, H., Ulutaş, B., Aypak S. (2008). Miks helmint infeksiyonlu keçilerde haptoglobin, serum amyloid A ve seruloplazmin konsantrasyonları. Türkiye Parazitololoji Dergisi, 32 (3), 229-233.
61. Ulutaş, B., Bayramlı, G., Ulutaş, P. A., Karagenc, T. (2005). Serum concentration of some acute phase proteins in naturally occurring canine babesiosis: preliminary studies. Veterinary Clinical Pathology, 34, 144-147. https://doi.org/10.1111/j.1939-165X.2005.tb00028.x
62. Yarım, G. F., Şinasi, U., Açıcı, M., Beyhan, Y. E. (2010). Kistik ekinokokozisli sığırlarda serum sialik asit düzeyleri. Ankara Üniversitesi Veteriner Fakültesi Dergisi, 57(1), 61-63. https://doi.org/10.1501/Vetfak_0000002311
63. Yıldız, K., Gürcan, S. (2003). Prevalence of Hydatidosis and fertility of Hydatid cysts in sheep in Kırıkkale, Turkey. Acta Veterinaria Hungarica, 51, 181-187. https://doi.org/10.1556/avet.51.2003.2.6
64. Yoshioka, T., Kawada, K., Shimada, T., Mori, M.(1979). Lipid peroxidation in maternal and cord blood and protective mechanism aganist activated-oxygen toxicity in the blood. American Journal of Obstetrics & Gynecology: Home Page, 135(3), 372-376. https://doi.org/10.1016/0002-9378(79)90708-7