Effect of lemon (Citrus lemon) pumace powder supplementation on growth performance, lipid peroxidation and protein oxidation biomarkers in some tissues of common carp (Cyprinus carpio)

Iranian Journal of Veterinary Science and Technology

مقاله 7، دوره 10، شماره 2 - شماره پیاپی 19، شهریور 2018، صفحه 55-63   

نوع مقاله: Research Articles

شناسه دیجیتال (DOI): 10.22067/veterinary.v2i10.73469

نویسندگان

Sara Safaeian laein؛ Amir salari؛ Davar Shahsavani^* ؛ Hasan Baghshani

Ferdowsi University of Mashhad

چکیده

The aim of this study was to evaluate the antioxidant potential of lemon pumace powder (peel and pulp), as an inexpensive and valuable source of nutrient in diet of common carp. Fish (60 ± 5 g) were divided randomly into four groups of 30 each. Group 1 fish were fed with basic diet, serving as the control. Fish in group 2 and 3 and 4 were fed the basic diet supplemented with 1.5%, 3% and 5% lemon pumace powder, respectively. Results showed that growth performance including final weight, weight gain (WG), feed conversion ratio (FCR) and specific growth rate (SGR) significantly increased as compared to control. Malondialdehyde (MDA) values of muscle significantly increased as compared to control in all treatment groups and the decreeing effect of lemon pumace powder on malondialdehyde (MDA) values of kidney and liver was only significant in group 4, when compared with the control group (p < 0.05). Protein carbonyl contents were significantly decreased in kidney and liver in group 3 and 4 as compared to control group and protein carbonyl of muscle significantly decreased as compared to control in all treatment groups. FRAP values of liver significantly increased only in group 3 as compared to control, and FRAP values of kidney and muscle significantly increased only in group 4 as compared to control (p < 0.05). These data suggest that supplementation of 5% lemon pumace powder to be more effective than its lower levels in strengthening the antioxidant system against oxidative stress.

کلیدواژه‌ها

Antioxidant؛ common carp؛ Lipid peroxidation؛ Protein carbonyls

مراجع

1. EFSA. Scientific opinion on dietary reference values for fats,

including saturated fatty acids, polyunsaturated fatty acids,

monounsaturated fatty acids, trans fatty acids, and cholesterol.

EFSA J. 2010;8:1461:1–107.

2. Simopoulos AP. Omega-3 fatty acids in health and disease

and in growth and development, a review. Am J Clin Nutr.

1991;54:438–463.

3. Richards M, Modra A, Li R. Role of deoxyhemoglobin in lipid

oxidation of washed cod muscle mediated by trout, poultry

and beef hemoglobins. Meat Sci. 2002;62:157–163.

4. Maqsood S, Benjakul S. Effect of bleeding on lipid oxidation

and quality changes of Asian seabass (Lates calcarifer) muscle

during iced storage. Food Chem. 2011;124:459–467.

5. Maqsood S, Benjakul S, Kamal-Eldin A. Haemoglobinmediated

lipid oxidation in the fish muscle: a review. Trends Food Sci

Technol. 2012;28:33–43.

6. Shacter E. Quantification and significance of protein oxidation

in biological samples. Drug Metab Rev. 2000;32:307–326.

7. Sie H, Stahl W, Sevanian A. Nutritional, dietary and postprandial

oxidative stress. J Nutr. 2005;135:969–972.

8. Welker T, Congleton J. Effect of dietary alphatocopherol +

ascorbic acid, selenium, and iron on oxidative stress in

sub-yearling Chinook salmon (Oncorhynchus tshawytscha

Walbaum). J Anim Physiol Anim Nutr. 2009;93:15–25.

9. Nakano T, Kanmuri T, Sato M, Takeuchi M. Effect of astaxanthin

rich red yeast (Phaffia rhodozyma) on oxidative stress

in rainbow trout. Biochim Biophys Acta. 1999;1426:119-125.

10. Agu P, Olerumi O, Tuleun C. Nutritional evalution of sweet

orange (citrus sinensis) fruit peel as feed resource in broiler

production. Inter J of Poul Sci. 2010;9:684-688.

11. Gomez B, Gullon R, Yañez H, Schols J. Prebiotic potential of

pectins and pectic oligosaccharides derived from lemon peel

wastes and sugar beet pulp: A comparative evaluation. J of Func Foods. 2016;20:108–121.

12. Sultana B, Anwar F, Iqbal S. Effect of different cooking methods on the

antioxidant activity of some vegetables

from Pakistan. J of. Food Sci and

Tech. 2010;43:20.

13. Smith G, Hole M. Browning of salted

sun-dried fish. J Sci Food Agric.

1991;55:291-301.

14. Benzie I, Strain J. The Ferric Reducing

Ability of Plasma (FRAP) as a Measure

of “Antioxidant Power: The FRAP Assay”.

Analy Biochem. 1996;239:70-76.

15. Basmacioglu H, Tokusoglu O, Ergul

M. The effect of oregano and rosemary

essential oils or alpha-tocopheryl

acetate on performance and lipid

oxidation of meat enriched with n-3

PUFA’s in broilers. Sou Afri J of Ani

Sci. 2004;34:197-210.

16. Botsoglou A, Grigoropoulou H, Botsogl

E, Govaris A, Papgeorgiol G. The

effects of dietary oregano essential

oil and α-tocopheryl acetate on lipid

oxidation in raw and cooked turkey

during refrigerated storage. Meat Sci.

2003;65:1193-1200.

17. Coetzee M, Hoffman M. Effect of dietary

vitamin E on the performance

of broilers and quality of broiler meat

during refrigerated and frozen storage.

S Afr J Anim. Sci. 2001;31:158–

173.

18. Lopez-bote J, Gray I, Gomma A, Flegal

J. Effect of dietary administration of

oil extracts from rosemary and sage

on lipid oxidation in broiler meat. Bri

Poul Sci. 1998;39:235-240.

19. Lau W, King J. Pre- and post-mortem

use of grape seed extract in dark

poultry meat to inhibit development

of thiobarbituric acid reactive substances.

J of Agri and Food Chem.

2003;51:1602-1607.

20. Tang Z, Kerry P, Sheehan D, Buckley

J, Morrissey A. Dietary tea catechins

and iron-induced lipid oxidation in

chicken meat, liver and heart. Meat

Sci. 2000;56:285-290.

21. Papageorgiou G, Botsoglu N, Govaris

A, Giannenas I, Iliadis S, Botsoglu E.

Effect of dietary oregano oil and α-tocopheryl

acetate supplementation on

iron-induced lipid oxidation of turkey

breast, thigh, liver and heart tissues.

J of Anim Phys and Anim Nutr.

2003;87:324-335.

22. Van Hai N. The use of medicinal plants

as immune stimulants in aquaculture:

A review Aqua. 2015;446:88–96.

23. Reverter M, Bontemps N, Lecchini

L, Banaigs B, Sasal P. Use of plant

extracts in fish aquaculture as an alternative

to chemotherapy. Current

status and future perspectives. Aqua.

2014;433:50–61.

24. Harikrishnan R, Balasundaram C, Heo

M. Impact of plant products on innate

and adaptive immune system of

cultured finfish and shellfish. Aqua.

2011;317:1–15.

25. Bulfon C, Volpatti D, Galeotti M. Current

research on the use of plant-derived

products in farmed fish. Aqua

Res. 2015;46:513–551.

26. Acar U, Kesbiç O, Yılmaz S, Gültepe N,

Türker A. Evaluation of the effects of

essential oil extracted from sweet orange

peel (Citrus sinensis) on growth

rate of tilapia (Oreochromis mossambicus)

and possible disease resistance

against Streptococcus iniae. Aqua.

2015;437:282-286.

27. Ngugi C, Oyoo-Okoth E, Muchiri M.

Effects of dietary levels of essential

oil (EO) extract from bitter limon

(Citrus limon) fruit peels on growth,

biochemical, haematoimmunological

parameters and disease resistance in

Juvenile Labeo victorianus fingerlings

challenged with Aeromonas hydrophila.

Aqua Res. 2016;1-13.

28. Ispır U, Yonar M, Oz O. Effect of dietary

vitamin E supplementation on

the blood parameters of nile tilapia

(Oreochromis niloticus). J Anim

Plant Sci. 2011;21:566–569.

29. Halliwell B, Whiteman M. Measuring

reactive species and oxidative damage

in vivo and in cell culture: how should

you do it and what do the results

mean? Br J Pharmacol. 2004;142:231–

255.

30. Disatnik M, Dhawan J, Yu Y, Beal M,

Whirl M, Franco A, Rando T. Evidence

of oxidative stress in mdx mouse muscle:

studies of the pre-necrotic state. J

Neurol Sci. 1998;161:77–84.

31. Kaczor J, Hall J, Payne E, Tarnopolsky

M. Low intensity training decreases

markers of oxidative stress in skeletal

muscle of mdx mice. Free Radic Biol

Med. 2007;43:145–154.

32. Zwart L, Meerman J, Commandeur

J, Vermeulen N. Biomarkers of free

radical damage: applications in experimental

animals and in humans. Free

Radic Biol Med. 1999;26:202–226.

33. Kadiiska M, Gladen B, Baird D, Germolec

D, Graham L, Parker C. Biomarkers

of oxidative stress study

II: are oxidation products of lipids,

proteins, and DNA markers of CCl

4 poisoning? Free Radic Biol Med.

2005;38:698–710.

34. Durak I, Aytac B, Atmaca Y, Devrim

E, Avci A, Erol C, Oral D. Effects of

garlic extract consumption on plasma

and erythrocyte antioxidant parameters

in atherosclerotic patients. Life

Sci. 2004;75:1959–1966.

35. Jabbari A, Argani H, Ghorbanihaghjo

A, Mahdavi R. Comparison between

swallowing and chewing of garlic on

levels of serum lipids, cyclosporine,

creatinine and lipid peroxidation in

renal transplant recipients. Lipids

Health Dis. 2005;4:11.

36. Duda G, Suliburska J, Pupek-Musialik

D. Effects of shortterm garlic supplementation

on lipid metabolism and

antioxidant status in hypertensive

adults. Pharmacol Rep. 2008;60:163–

170.

37. Imai I, Ide N, Nagae S, Moriguchi T,

Matsuura H, Itakura Y. Antioxidant

and radical scavenging effects of aged

garlic extract and its constituents.

Planta Med. 1994;60:417–420.

38. Hfaiedh N, Murat J, Elfeki A. Compared

ability of garlic (Allium sativum)

extract or alpha-tocopherol?

magnesium association to reduce

metabolic disorders and oxidative

stress in diabetic rats. Phytother Res.

2010;25:821–827.

39. Nahdi A, Hammami I, Kouidhi W,

Chargui A, Ben Ammar A, Hamdaoui

M, El May A, El May M. Protective

effects of crude garlic by reducing

iron-mediated oxidative stress, proliferation

and autophagy in rats. J Mol

Histol. 2010;41:233–245.

40. Vidyashankar S, Sambaiah K, Srinivasan

K. Effect of dietary garlic and

onion on biliary proteins and lipid

peroxidation which influence cholesterol

nucleation in bile. Steroids.

2010;75:272–281.

41. Kumar P, Prasad Y, Patra A, Ranjan

R, Swarup D, Patra R, Pal S. Ascorbic

acid, garlic extract and taurine

alleviate cadmium-induced oxidative

stress in freshwater catfish (Clarias

batrachus). Sci Total Environ.

2009;407:5024–5030.

42. Banerjee S, Maulik M, Manchanda

C, Dinda A, Das T, Maulik S. Garlic-

induced alteration in rat liver

and kidney morphology and associated

changes in endogenous antioxidant

status. Food Chem Toxicol.

2001;39:793–797.

43. Mohebbi A, Nematollahi A, Ebrahimi

Dorcheh E, Goodarzian Asad F. Influence

of dietary garlic (Allium sativum)

on the antioxidative status of

rainbow trout (Oncorhynchus myki

ss). Aquacult Res. 2012;43:1184–1193.

44. Chen H, Tsai C, Yang J, Liu C, Kuo W,

Lii K. The combined effects of garlic

oil and fish oil on the hepatic antioxidant

and drug-metabolizing enzymes

of rats. Br J Nutr. 2003;89:189–200.

45. Maldonado P, Barrera D, Medina-

Campos O, Herna´ndez- Pando R,

Ibarra-Rubio M, Pedraza-Chaverrı

´ J. Aged garlic extract attenuates

gentamicin induced renal damage

and oxidative stress in rats. Life Sci.

2003;73:2543–2556.

46. Mercier Y, Gatellier P, Renerre M. Lipid

and protein oxidation in vitro, and

antioxidant potential in meat from

Charolais cows finished on pasture

or mixed diet. Meat Sci. 2004;66:467–

473.

47. Srinivasan S, Hultin H. Hydroxyl radical

modification of fish muscle proteins.

J Food Biochem. 1995;18:405–

425.

48. Petron M, Raes K, Claeys E, Lourenc

M, Fremaut D, De Smet S. Effect of

grazing pastures of different botanical

composition on antioxidant enzyme

activities and oxidative stability of

lamb meat. Meat Sci. 2007;75:737–

745.

49. Velasco V, Williams P. Improving meat

quality through natural antioxidants.

Chil J of Agric Res. 2011;71(2):313-

322.

50. Norazalina S, Norhaizan M, Hairuszah

I, Norashareena M. Anticarcinogenic

efficacy of phytic acid extracted from

rice bran on azoxymethane-induced

colon carcinogenesis in rats. Exper

Toxi Pathol. 2010;62:259-268.

51. Dudonne S, Vitrac X, Coutiere P,

Woillez M, Merillon M. Comparative

study of antioxidant properties

and total phenolic content of 30 plant

extracts of industrial interest using

DPPH, ABTS, FRAP, SOD, and ORAC

assays. J of Agri and Food Chem.

2009;57: 1768–1774.

52. Jose Maria G, Cristobal Espinosa M,

Francisco A, Guardiola M, Ángeles

Esteban C. Dietary dehydrated

lemon peel improves the immune but

not the antioxidant status of gilthead

seabream (Sparus aurata L.). Fish and

Shellfish Immu. 2017; doi: 10.1016/j.

fsi.2017;03.042.

53. Naeiji N, Shahsavani D, Baghshani H.

Effect of dietary garlic supplementation

on lipid peroxidation and protein

oxidation biomarkers of tissues as well

as some serum biochemical parameters

in common carp Cyprinus carpio.

Fish Sci. 2013; 79:4.