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Protective effect of soursop (Annona muricata linn.) juice on oxidative stress in heat stressed rabbits

Protective effect of soursop (Annona muricata linn.) juice on oxidative stress in heat stressed... Background: Preventing oxidative stress in heat stressed animals may be possible by increasing antioxidant defence via exogenous administration of antioxidant substrate and/or its precursors. The study aimed to investigate the effect of Soursop juice in mitigating oxidative stress induced by heat stress in rabbit. Methods: Sixty mixed breed rabbit bucks aged 12–18 months old with the average weight of 1826 ± 8.35 g/ rabbit, randomly allotted to experimental treatments of four replicates each, in a completely randomized design during high-temperature humidity index in Ado Ekiti, Southwest Nigeria. Soursop juice (SSJ) was administered via oral −1 drenched daily per kg body weight (BW), to designated treatment 1 to 5; 0.55 mlkg BW distilled water (control), 0.55 −1 −1 −1 −1 mlkg BW SSJ, 1.11 mlkg BW SSJ, 1.67 mlkg BW SSJ and 2.22 mlkg BW SSJ, respectively. Fastened blood samples were collected at days 28 and 56, and assay for serum protein, cholesterol, triglycerides, superoxide dismutase, catalase, reduced glutathione and lipid peroxidation using standard procedures. Result: Result revealed that SSJ demonstrated hypocholesterolemic effect in a dose-dependent manner throughout the study. Effect of chronic administration of SSJ to heat stressed rabbits proved beneficial, as SSJ reduced serum lipid peroxidation and enhanced antioxidant activity over 8 weeks. −1 Conclusion: Administration of soursop juice to heat-stressed bucks at 2.22 mlkg BW offered optimum antioxidant defense against oxidative stress. Keywords: Antioxidants, Glutathione, Heat stress, Lipid peroxide, Rabbit, Soursop Background species and its metabolites (ROS-M) accumulation in Heat stress is one of the most important stressors espe- blood and seminal fluid of bucks during heat stress [2]. cially in hot regions of the world. Effects of heat stress The accumulations of ROS-M in the biological system is on rabbits bucks has been widely documented to include a resultant of decline in antioxidant defense system, not- reduced productivity, compromised the immune system, ably enzymatic antioxidants and total antioxidant activ- collapse inefficient thermoregulatory mechanism and re- ity. The endogenous production of antioxidant enzymes duce fertility when environmental variables induce heat and the total antioxidant activity of rabbit bucks decline stress [1]. Most recently, exotic breeds of rabbit were in- in huge proportion when animals experience heat stress troduced to Nigeria, to improve rabbit population in the compared to when the environmental variables depict region. It was observed that oxidative stress greatly com- the absence of heat stress [3]. promised animal physiology, with high reactive oxygen Jimoh et al., [2] reported that mitigating strategies to ameliorate the adverse effects of heat stress in rabbits are imperative for productivity. The possibility of increasing * Correspondence: abubakarjimoh2011@gmail.com Department of Agricultural Technology, Federal Polytechnic Ado Ekiti, Ado antioxidant defence through exogenous administration of Ekiti, Ekiti State, Nigeria antioxidant substrate and/or its precursors requires Full list of author information is available at the end of the article © The Author(s). 2018 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Jimoh et al. Journal of Animal Science and Technology (2018) 60:28 Page 2 of 6 investigation. Soursop (Annona muricata.L.) belongs to rabbit house has natural lighting program (12D:12 L), with the family Annonaceae which is found throughout the tro- the dynamic ventilation system. The experimental units pics. Several studies have described the medicinal pur- are made of wire mesh double sided boxes of 1.1sq.m. poses of Annona muricata fruit, leaf, bark, and seed; The animals were fed ad libitum with diets containing sedative, antispasmodic, hypoglycemic, hypotensive, crude protein 17.05%, digestible energy 2592.06 Kcal/kg, smooth muscles relaxant and nervine, cytotoxic against crude fibre 10.02%, calcium 0.45% and phosphorus 0.21% cancer cells. Soursop possess protective and beneficial ef- as shown in Table 1. Freshwater was made available to the fect against oxidative stress in rats by decreasing lipid per- animals always. Other routines and periodic management oxidation and enhancing endogenous antioxidants [4]. practices necessary for rabbit production were carried out. These prove as a potential candidate to mitigate oxidative The bucks were adult of 12-18 months old with the stress induced by heat stress in the rabbit in the tropics. average weight of 1826 ± 8.35 g. 60 bucks were randomly This study investigates the protective effect of soursop juice allotted to five experimental treatments of four replicates against heat stress-induced oxidative stress in rabbit bucks. (3 bucks per replicate) per treatment in a completely ran- domised design. SSJ was administered per kg body weight Methods (BW), designated as treatment 1 to 5, administered −1 −1 The study was conducted at the rabbit unit of Teaching 0.55mlkg BW distilled water (control), 0.55 mlkg BW −1 −1 and Research Farm, Department of Agricultural Technol- SSJ, 1.11 mlkg BW SSJ, 1.67 mlkg BW SSJ and 2.22 −1 ogy, Federal Polytechnic, Ado-Ekiti, Nigeria. The study mlkg BW SSJ respectively. Each treatment consists of 12 area is located between latitude 7 3′7″N7′12″N and lati- bucks. The soursop juice was administered orally to the o o tude 5 11″Eand 5 31″E. The temperature-humidity rabbit in the morning between 8:00 am and 8:30 am daily index (THI), an indicator of thermal comfort level for ani- to all bucks in a study that lasted for eight weeks. mals in an enclosure was calculated as modified by Marai et al. [5] and given as: Sample collection and analysis A baseline blood sample was collected from all rabbits at THI ¼ t−½ðÞ 0:31  0:31 x RH t  14:4 least temperature humidity index, to serve as positive Table 1 Gross composition of experimental diet Where RH = relative humidity /100. t = ambient temperature. Ingredient Inclusion (g/100 g) The values of THI obtained for rabbit are classified as: Maize 25 < 27.8 °C = absence of heat stress, Wheat offal 5 27.8–28.9 °C = moderate heat stress, Rice bran 6 28.9–30 °C = severe heat stress and. BDG 5 above 30 °C = very severe heat stress (Marai et al.,) [5]. SBM 17 The study was conducted between December 2017 Groundnut haulms 40 and January 2018 with average daily THI of 29.94 ± 1.56 and 28.59 ± 3.10 at the rabbit unit, which is the peak of Methionine 0.4 the dry season in the study area at the time. Lysine 0.1 Bone meal 1 Collection and extraction of soursop juice Premix 0.25 Ripe soursop (Annona muricata) fruit was harvested fresh Salt 0.25 and it was extracted in the Teaching and Research Farm Total 100 of the Agricultural Technology, Federal Polytechnic Ado –Ekiti, Nigeria. The fruits were peeled, weighed and the Calculated nutrient composition fruit pulp blended (without the seeds) with the ratio of 1:2 Dry matter (%) 87.87 (pulp: distilled water). The soursop juice was clarified with Crude protein (%) 16.44 juice extractor (Mikachi model No 1706). The juice Digestible energy (kcal/kg) 2717.86 obtained was designated as soursop juice (SSJ) and kept Ether extract (%) 3.34 frozen 4 °C in disposable 5 ml sterile sample bottles until Crude fibre (%) 16.48 its required for use. Lysine (%) 1.01 Experimental animal and management Methionine (%) 0.75 Sixty (60) mixed breed (New Zealand white x Chinchilla) Calcium (%) 1.60 male rabbit bucks kept in a battery cage system kept in an Phosphorus (%) 0.45 open-sided house were used for the experiment. The Jimoh et al. Journal of Animal Science and Technology (2018) 60:28 Page 3 of 6 th control as non-heat stressed treatment. The fastened the overall mean for each character; B is the fixed effect of i −1 blood sample was collected at 28 days and 56 days of the Soursop (SSJ) was administered 5 levels (i=0.55 mlkg BW −1 −1 study. Blood was collected through the marginal ear vein water (control), 0.55 mlkg BW SSJ, 1.11 mlkg BW −1 −1 into a sample bottle. Serum was separated by centrifuga- SSJ, 1.67 mlkg BW SSJ and 2.22 mlkg BW SSJ); and tion (Medi Scan centrifuge model No 800D) and stored at e is the random residual effect. ijl -2 °C before analysis. Serum obtained was assayed for total protein, albumin, cholesterol, and triglyceride Results using commercial assay kits and its procedure, lipid Serum oxidative status of non-heat stressed treatment peroxidation, reduced glutathione, catalase, and super- is shown in Table 2. Total protein, antioxidant activities oxide dismutase activity using standard procedures. were higher than values obtained in heat stressed Superoxide dismutase (SOD); to 2.1 ml of 50 m M groups. However, cholesterol and lipid peroxidation butter, 0.02 ml of enzyme source and 0.86 ml of distilled were lower in non-heat stressed group compared with water. The reaction is initiated with 0.02 ml of 10 mM heat stressed groups. pyrogallol and change in absorbance monitored at 420 mm. One unit of SOD is defined as that amount of enzyme required to inhibit to auto-oxidation of pyrogal- Serum oxidative status of heat-stressed bucks gavaged lol by 50℅ in standard assay system of 3 ml. The spe- with soursop juice cific activity is expressed as unit /min/mg protein. Serum oxidative status of heat stressed bucks gavaged Catalase activity; the assay system contain 1.9 ml,0.05 M with soursop juice for 4 weeks is shown in Table 3.The buffer PH 7.0 and 1.0 ml 0.059 M water. The reaction is serum total protein of bucks on control were statistically initiated by addition of 0.1 ml enzyme source. The (p > 0.05) similar with bucks on treatments 3, 4 and 5. decrease in absorbance is monitored at 1 min interval Cholesterol of bucks on SSJ based treatments were for 5 min at 240 min and activity is expressed as moles significantly (p < 0.05) lower than those on treatment of water decomposed /min/mg protein. 1. Triglyceride declined with increased SSJ adminis- The assay for lipid peroxidation; The reaction mixture tration. Bucks on treatments 2, 3, 4 and 5 had signifi- in a total volume of 3.0 ml contained 1.0 ml serum, cantly (p < 0.05) low values while bucks not offered 1.0 ml of TCA (0.67%). All the test tubes were placed in SSJ had the statistically highest value. Serum lipid a boiling water bath for a period of 45 min. The tubes peroxidation was significantly (p < 0.05) highest in the were shifted to the ice bath and then centrifuged at buck on control and least in bucks offered treatments 4 2500 rpm for 10 min. The amount of malondialdehyde and 5. However, bucks on treatments 2 and 3 had statisti- (MDA) formed in each of the samples was assessed by cally (p > 0.05) similar lipid peroxidation values and were measuring the optical density of the supernatant at significantly (p < 0.05) higher than bucks on treatments 4 532 nm. and 5. Glutathione of bucks on treatments 4 and 5 was The glutathione (GSH) content; in which 1.0 ml of significantly (p < 0.05) highest across the treatments with PMS fraction (10%) was mixed with 1.0 ml of sulphosa- significantly least values obtained in bucks on treatments licylic acid (4%).The sample was incubated at 4 °C for at 1 and 2. Superoxide dismutase activity was highest statisti- least 1 h and then subjected to centrifugation at cally in bucks on treatment 5, with bucks on treatments 1 1200 rpm for 15 min at 4 °C. The assay mixture con- and 2 having the significantly (p < 0.05) least values. Bucks tained 0.4 ml filtered aliquot, 2.2 ml phosphate, buffer on treatment 3 and 4 had lower SOD than bucks on treat- (0.1 M, PH 7.4) and 0.4 ml DTNB (10 mM) in a total ment 5. Serum catalase activity in SSJ based groups was volume of 3.0 ml. The yellow colour developed was read significantly higher than the control. immediately at 412 mm. Table 2 baseline of serum oxidative status of the experimental rabbits at absence of heat stress Statistical analysis Parameters Baseline assessment Data obtained were subjected to analysis of variance at (un-heat stressed treatment) α = 0.05, the general linear model procedure of SAS, Total Protein (g/dL) 54.8 while means were separated using Duncan’s multiple Cholesterol (mg/dL) 51.04 range test of same software. Triglyceride (mg/dL) 114.53 The statistical model is as the following: Lipid Peroxidation (TBARS/mg protein) 0.09 Y ¼ μ þ B þ e ijl i ijl Glutathione (μg GSH /min/mg protein) 54.05 Catalase (nm H O /min/mg protein) 132.77 2 2 Where Y represents the value of serum biochemical pa- ijl Superoxide Dismutase (U/min/mg protein) 78.68 th rameters and oxidative status measured in the l animal; μ is Jimoh et al. Journal of Animal Science and Technology (2018) 60:28 Page 4 of 6 Table 3 Serum oxidative status of heat stressed bucks gavaged with soursop juice for 4 weeks Treatment 1 Treatment 2 Treatment 3 Treatment 4 Treatment 5 SEM − 1 − 1 − 1 − 1 −1 (0 mlkg BW) (0.55 mlkg BW) (1.11 mlkg BW) (1.67 mlkg BW) (2.22 mlkg BW) a b a a a Total Protein (g/dL) 54.8 14.92 8.57 14.28 13.18 11.10 1.24 a b b b b Cholesterol (mg/dL) 51.04 61.17 48.26 46.95 50.47 50.88 3.86 a b c c c Triglyceride (mg/dL) 114.53 148.01 129.61 103.49 103.31 99.52 9.09 a b b c c Lipid Peroxidation 0.09 1.46 0.90 0.96 0.79 0.75 0.05 (TBARS/mg protein) c c b a a Glutathione 54.05 17.39 20.90 27.08 33.86 38.46 3.48 (μg GSH /min/mg protein) b a a a a Catalase 132.77 54.01 95.05 87.38 90.02 96.50 6.38 (nm H O /min/mg protein) 2 2 c c b b a Superoxide Dismutase 78.68 21.74 24.64 35.87 38.26 60.63 3.62 (U/min/mg protein) Different superscipt denote statistically significant differences at p ≤ 0.05 Serum oxidative status of heat stressed bucks gavaged Discussion with soursop juice for 8 weeks (Table 4) reveal that Cholesterol and triglyceride values of SSJ drenched bucks serum total protein in bucks on treatments 3, 4 and 5 were lower than the control over 8 weeks. This shows that are statistically similar and significantly (p < 0.05) lower SSJ demonstrated the hypocholesterolemic effect in a than bucks on treatments 1 and 2. Serum cholesterol dose-dependent manner throughout the study, as evident of bucks on treatments 1, 2 and 3 are similar and in cholesterol and triglyceride values. This corroborates were statistically (p < 0.05) higher than bucks on treat- reports that A. muricata lowers hypertriglyceridemia and ment 4 and 5. Triglyceride of bucks on control was hypercholesterolemia in alloxan-induced diabetic rats [6]. significantly (p < 0.05) higher than bucks on SSJ based Zheng et al. [7] demonstrated that fruit and vegetable treatments. Serum lipid peroxidation of bucks on juice reduce total cholesterol in the body and improve treatment 1 was significantly (p < 0.05) highest, while cholesterol profile in the blood. The improving blood bucks on treatment 5 had significantly (p < 0.05) least lipids effects of the juice blend were attributed to the high values. Serum glutathione activity of bucks on SSJ content of total polyphenol. The trend of result shows that treatments were statistically similar and significantly total protein of SSJ drenched bucks was lower than (p < 0.05) higher than bucks on control. Serum cata- control and increase across the treatments with the period lase activity in SSJ based groups was significantly of administration. higher than the control. Superoxide dismutase activity SSJ reduced serum lipid peroxidation throughout the of bucks on treatment 1, 2, 3 and 4 was statistically study, this proves a beneficial effect of chronic adminis- similar and significantly (p < 0.05) lower than SOD of tration of SSJ on heat stressed bucks. This is revealed by buck on treatment 5. values of lipid peroxidation in SSJ drenched bucks, Table 4 Serum oxidative status of heat stressed bucks gavaged with soursop juice for 8 weeks Baseline assessment Treatment 1 Treatment 2 Treatment 3 Treatment 4 Treatment 5 SEM −1 −1 − 1 − 1 − 1 (un-heat stressed (0 mlkg BW) (0.55 mlkg BW) (1.11 mlkg BW) (1.67 mlkg BW) (2.22 mlkg BW) treatment) a a b b b Total Protein (g/dL) 54.8 43.39 39.20 32.70 29.60 24.15 2.27 a a a b b Cholesterol (mg/dL) 51.04 57.91 50.19 51.91 41.03 36.68 2.97 a b b b b Triglyceride (mg/dL) 114.53 214.78 134.15 177.05 155.75 129.77 10.89 a b b b c Lipid Peroxidation 0.09 1.41 0.35 0.38 0.29 0.19 0.04 (TBARS/mg protein) b a a a a Glutathione (μg GSH 54.05 27.79 37.28 38.01 45.31 45.99 4.29 /min/mg protein) b a a a a Catalase (nm H O 132.77 43.58 102.42 100.89 103.36 109.03 7.29 2 2 /min/mg protein) b b b b a Superoxide Dismutase 78.68 17.39 20.29 19.57 21.74 28.70 3.01 (U/min/mg protein) Different superscipt denote statistically significant differences at p ≤ 0.05 Jimoh et al. Journal of Animal Science and Technology (2018) 60:28 Page 5 of 6 which were lower at 8 weeks than at 4 weeks of the [11]. This study also agrees with the notion that study. This reveals that the duration of administration of antioxidant-rich juice/extracts are more effective when the SSJ enhanced mitigation of oxidant accumulations and/ body has undergone intense, long-term oxidative stress, or production in heat stressed bucks. Hypercholesterol- rather than in healthy individuals or in individuals under- emia is related to increased lipid peroxidation [7], thus going short-term or acute oxidative stress [11]. Zheng et the mechanism of soursop juice reduction of cholesterol al. [7] review antioxidant effects of several fruits and contributes to lowering lipid peroxidation as revealed in vegetable juice and concluded that the consumption of this work. Similarly, cranberry powder has been shown juice enhanced total antioxidant activity and enzymatic to decrease the accumulation of malondialdehyde antioxidants and are important therapies to ameliorate (MDA, an indicator of oxidative damage) in male New oxidative stress and its related diseases. Similarly, Syahida Zealand rabbit kidneys [8]. This is also supported by et al. [12]reportedthat Annona muricata L. extract claims that A. muricata extract has a protective and contains the high total antioxidant, which improved the beneficial effect on hepatic tissues subjected to STZ- total antioxidant status of Sprague-Dawley rats as the induced oxidative stress, by decreasing lipid peroxidation dosage increased, which is good in promoting health. and indirectly enhancing production of insulin and endogenous antioxidants [4]. Conclusion Glutathione activity in heat stressed bucks in- This study reveals that chronic oral administration of creased with the dosage of SSJ administration at soursop juice proved beneficial in promoting good 4 weeks. However, at 8 weeks though values were health of heat-stressed bucks. Soursop juice reduced higher than at 4 weeks, the effect of the accumula- serum lipid peroxidation and enhanced antioxidant tion of production of glutathione could account for activity in heat stressed rabbit over 8 weeks. Administra- their similar values in SSJ drenched groups. The tion of soursop juice to heat-stressed bucks at 2.22 −1 least values of glutathione were obtained in control mlkg BW offered optimum antioxidant defense against group throughout the study, this demonstrates the oxidative stress. enhancement of glutathione activity in heat stressed Abbreviations bucks by SSJ to counteract the accumulation of BW: Body weight; GSH: Glutathione; MDA: Malondialdehyde; ROS-M: Reactive hydrogen peroxide. This is also observed in catalase oxygen species and its metabolites; SAS: Statistical analysis software; SOD: Superoxide dismutase; SSJ: Soursop juice; THI: Temperature- activity of the bucks, catalase and glutathione are re- humidity index sponsible for the elimination of hydrogen peroxide in biological systems. Similarly, ginger also a natural anti- Acknowledgements The authors appreciate the Teaching and Research Farm, Department of oxidant spice has been reported to decrease lipid peroxi- Agricultural Technology, Federal Polytechnic, Ado-Ekiti, Nigeria, for making dation, increasing GSH content and maintaining normal available animals for the research. We are grateful to Kolawole Khadijah levels of antioxidant enzymes in rats [9]. Effect of chronic Abidemi and Abiola Saheed Olajide for the care and handling of the animals, and their resourcefulness to the study. antioxidant-rich fruit administration was also reported by Kota et al. [10] in rat supplemented ginger for one month, Funding which recorded significant increases in activity of antioxi- This research did not receive any specific grant from any funding agency in the public, commercial or not-for profit sector. dant enzymes (superoxide dismutase, glutathione peroxid- ase, and catalase) in the liver. Superoxide dismutase Availability of data and materials activity was higher at 4 weeks in SSJ drenched bucks than “The study was undertaken with approval from institutional ethics committee for care and use of animal for research of the Federal polytechnic Ado Ekiti.” at 8 weeks. This could be due to the first line defense of SOD to convert superoxide anion to hydrogen peroxide in Authors’ contributions heat stressed bucks at 4 weeks. After regulating super- JOA designed and supervised the study, carried out statistical analysis and wrote the first manuscript. AES co supervised the study and wrote the oxide anion production and elimination, SOD activity de- experimental layout. ASO and OIS carried out the field work, OWO clines to favour catalase and glutathione activity at the carried out the laboratory assay, ODO and DOT approved the experimental latter stage, to counteract the hydrogen peroxide being protocol, read and corrected the first manuscript. All authors read and approve the final manuscript. produced as a metabolite of SOD. It suggests that SOD functions in tandem with catalase and glutathione regulate Ethical approval superoxide anion and hydrogen peroxide productions This research was undertaken with approval from institutional ethics committee of the Department of Agricultural Technology, Federal and/or accumulation in the bucks. This result in mitigat- Polytechnic, Ado-Ekiti. The institutional and national standards for the care and ing oxidants (lipid peroxides) and prevent oxidative stress use of animals for research in the Research Policy Handbook of the Federal in heat stressed bucks. This demonstrates SSJ mechanism Polytechnic, Ado-Ekiti were followed and appropriate measures were taken to minimize pain or discomfort on the animals. to mitigate oxidative stress in heat stressed bucks. Contrariwise, cranberry and ginger had no effect on the Consent for publication oxidative stress or antioxidant status in exercising horses Not applicable. Jimoh et al. Journal of Animal Science and Technology (2018) 60:28 Page 6 of 6 Competing interests The authors declare that there are no competing interests to the publication of this article. Publisher’sNote Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations. Author details Department of Agricultural Technology, Federal Polytechnic Ado Ekiti, Ado Ekiti, Ekiti State, Nigeria. Department of Science Technology, Federal Polytechnic, Ado Ekiti, Ekiti State, Nigeria. Department of Animal Science, Adekunle Ajasin University Akungba Akoko, Akungba Akoko, Ondo State, Nigeria. Received: 25 September 2018 Accepted: 2 November 2018 References 1. Jimoh OA, Ewuola EO. Thermoregulatory response of exotic rabbit breeds during peak temperature humidity index of Ibadan. Tropical Animal Production investigation. 2016;19(1):41–7. 2. Jimoh OA, Ewuola EO, Balogun AS. Oxidative stress markers in exotic breeds of rabbit during peak of heat stress in Ibadan, Nigeria. Journal of Advances in Biology and Biotechnology. 2017;12(1):1–9. https://doi.org/10.9734/JABB/ 2017/30437. 3. Jimoh OA. Assessment of the oxidative stress markers and reproductive performance of four exotic breeds of rabbit in Ibadan. Ph.D. Thesis 2016, University of Ibadan, Ibadan, Nigeria. 4. Adewole SO,Ojewole JAO. Protective effects of Annona muricata linn. (annonaceae) leaf aqueous extract on serum lipid profiles and oxidative stress in hepatocytes of streptozotocin-treated diabetic rats. Afr. J. Traditional, Complementary and Alternative Medicines 2009, 6 (1): 30–41. 5. Marai IFM, Ayyat MS. Abd El-MonemUM. Growth performance and reproductive traits at first parity of New Zealand white female rabbits as affected by heat stress and its alleviation, under Egyptian conditions. Trop Anim Health Prod. 2001;33:1–12. 6. Sawant TP, Gogle DP. A brief review on recent advances in clinical research of Annona muricata. International journal of universal pharmacy and bio. Sciences. 2014;3(3):267–304. 7. Zheng J, Zhou Y, Li S, Zhang P, Zhou T, D X, Li H. Review effects and mechanisms of fruit and vegetable juices on cardiovascular diseases. Int J Mol Sci. 2017;18(555):1–15. https://doi.org/10.3390/ijms18030555. 8. Han CH, Kim SH, Kang SH, Shin OR, Lee HK, Kim HJ, Cho YH. Protective effects of cranberries on infected-induced oxidative renal damage in a rabbit model of vesico-ureteric reflux. BJU Int. 2007;100:1172–5. 9. Ahmed RS, Seth V, Pasha ST, Banerjee BD. Influence of dietary ginger (Zingiber Officinale Rosc) on oxidative stress induced by malathion in rats. Food Chem Toxicol. 2000;38:443–50. 10. Kota N, Krishna P, Polasa K. Alterations in antioxidant status of rats following intake of ginger through diet. Food Chem. 2008;106:991–6. 11. Smarsh DN, Liburt N, Streltsova J, Mckeever K, Williams CA. Oxidative stress and antioxidant status in intensely exercising horses administered nutraceutical extracts. Equine Vet J. 2010;42(Suppl. 38):317–22. https://doi. org/10.1111/j.2042-3306.2010.00182.x. 12. Syahida M, Maskat MY, Suri R, Mamot S, Hadijah H. Soursop (Annona muricata L.): blood hematology and serum biochemistry of Sprague-Dawley rats. Int Food Res J. 2012;19(3):955–9. http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Journal of Animal Science and Technology Springer Journals

Protective effect of soursop (Annona muricata linn.) juice on oxidative stress in heat stressed rabbits

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Abstract

Background: Preventing oxidative stress in heat stressed animals may be possible by increasing antioxidant defence via exogenous administration of antioxidant substrate and/or its precursors. The study aimed to investigate the effect of Soursop juice in mitigating oxidative stress induced by heat stress in rabbit. Methods: Sixty mixed breed rabbit bucks aged 12–18 months old with the average weight of 1826 ± 8.35 g/ rabbit, randomly allotted to experimental treatments of four replicates each, in a completely randomized design during high-temperature humidity index in Ado Ekiti, Southwest Nigeria. Soursop juice (SSJ) was administered via oral −1 drenched daily per kg body weight (BW), to designated treatment 1 to 5; 0.55 mlkg BW distilled water (control), 0.55 −1 −1 −1 −1 mlkg BW SSJ, 1.11 mlkg BW SSJ, 1.67 mlkg BW SSJ and 2.22 mlkg BW SSJ, respectively. Fastened blood samples were collected at days 28 and 56, and assay for serum protein, cholesterol, triglycerides, superoxide dismutase, catalase, reduced glutathione and lipid peroxidation using standard procedures. Result: Result revealed that SSJ demonstrated hypocholesterolemic effect in a dose-dependent manner throughout the study. Effect of chronic administration of SSJ to heat stressed rabbits proved beneficial, as SSJ reduced serum lipid peroxidation and enhanced antioxidant activity over 8 weeks. −1 Conclusion: Administration of soursop juice to heat-stressed bucks at 2.22 mlkg BW offered optimum antioxidant defense against oxidative stress. Keywords: Antioxidants, Glutathione, Heat stress, Lipid peroxide, Rabbit, Soursop Background species and its metabolites (ROS-M) accumulation in Heat stress is one of the most important stressors espe- blood and seminal fluid of bucks during heat stress [2]. cially in hot regions of the world. Effects of heat stress The accumulations of ROS-M in the biological system is on rabbits bucks has been widely documented to include a resultant of decline in antioxidant defense system, not- reduced productivity, compromised the immune system, ably enzymatic antioxidants and total antioxidant activ- collapse inefficient thermoregulatory mechanism and re- ity. The endogenous production of antioxidant enzymes duce fertility when environmental variables induce heat and the total antioxidant activity of rabbit bucks decline stress [1]. Most recently, exotic breeds of rabbit were in- in huge proportion when animals experience heat stress troduced to Nigeria, to improve rabbit population in the compared to when the environmental variables depict region. It was observed that oxidative stress greatly com- the absence of heat stress [3]. promised animal physiology, with high reactive oxygen Jimoh et al., [2] reported that mitigating strategies to ameliorate the adverse effects of heat stress in rabbits are imperative for productivity. The possibility of increasing * Correspondence: abubakarjimoh2011@gmail.com Department of Agricultural Technology, Federal Polytechnic Ado Ekiti, Ado antioxidant defence through exogenous administration of Ekiti, Ekiti State, Nigeria antioxidant substrate and/or its precursors requires Full list of author information is available at the end of the article © The Author(s). 2018 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Jimoh et al. Journal of Animal Science and Technology (2018) 60:28 Page 2 of 6 investigation. Soursop (Annona muricata.L.) belongs to rabbit house has natural lighting program (12D:12 L), with the family Annonaceae which is found throughout the tro- the dynamic ventilation system. The experimental units pics. Several studies have described the medicinal pur- are made of wire mesh double sided boxes of 1.1sq.m. poses of Annona muricata fruit, leaf, bark, and seed; The animals were fed ad libitum with diets containing sedative, antispasmodic, hypoglycemic, hypotensive, crude protein 17.05%, digestible energy 2592.06 Kcal/kg, smooth muscles relaxant and nervine, cytotoxic against crude fibre 10.02%, calcium 0.45% and phosphorus 0.21% cancer cells. Soursop possess protective and beneficial ef- as shown in Table 1. Freshwater was made available to the fect against oxidative stress in rats by decreasing lipid per- animals always. Other routines and periodic management oxidation and enhancing endogenous antioxidants [4]. practices necessary for rabbit production were carried out. These prove as a potential candidate to mitigate oxidative The bucks were adult of 12-18 months old with the stress induced by heat stress in the rabbit in the tropics. average weight of 1826 ± 8.35 g. 60 bucks were randomly This study investigates the protective effect of soursop juice allotted to five experimental treatments of four replicates against heat stress-induced oxidative stress in rabbit bucks. (3 bucks per replicate) per treatment in a completely ran- domised design. SSJ was administered per kg body weight Methods (BW), designated as treatment 1 to 5, administered −1 −1 The study was conducted at the rabbit unit of Teaching 0.55mlkg BW distilled water (control), 0.55 mlkg BW −1 −1 and Research Farm, Department of Agricultural Technol- SSJ, 1.11 mlkg BW SSJ, 1.67 mlkg BW SSJ and 2.22 −1 ogy, Federal Polytechnic, Ado-Ekiti, Nigeria. The study mlkg BW SSJ respectively. Each treatment consists of 12 area is located between latitude 7 3′7″N7′12″N and lati- bucks. The soursop juice was administered orally to the o o tude 5 11″Eand 5 31″E. The temperature-humidity rabbit in the morning between 8:00 am and 8:30 am daily index (THI), an indicator of thermal comfort level for ani- to all bucks in a study that lasted for eight weeks. mals in an enclosure was calculated as modified by Marai et al. [5] and given as: Sample collection and analysis A baseline blood sample was collected from all rabbits at THI ¼ t−½ðÞ 0:31  0:31 x RH t  14:4 least temperature humidity index, to serve as positive Table 1 Gross composition of experimental diet Where RH = relative humidity /100. t = ambient temperature. Ingredient Inclusion (g/100 g) The values of THI obtained for rabbit are classified as: Maize 25 < 27.8 °C = absence of heat stress, Wheat offal 5 27.8–28.9 °C = moderate heat stress, Rice bran 6 28.9–30 °C = severe heat stress and. BDG 5 above 30 °C = very severe heat stress (Marai et al.,) [5]. SBM 17 The study was conducted between December 2017 Groundnut haulms 40 and January 2018 with average daily THI of 29.94 ± 1.56 and 28.59 ± 3.10 at the rabbit unit, which is the peak of Methionine 0.4 the dry season in the study area at the time. Lysine 0.1 Bone meal 1 Collection and extraction of soursop juice Premix 0.25 Ripe soursop (Annona muricata) fruit was harvested fresh Salt 0.25 and it was extracted in the Teaching and Research Farm Total 100 of the Agricultural Technology, Federal Polytechnic Ado –Ekiti, Nigeria. The fruits were peeled, weighed and the Calculated nutrient composition fruit pulp blended (without the seeds) with the ratio of 1:2 Dry matter (%) 87.87 (pulp: distilled water). The soursop juice was clarified with Crude protein (%) 16.44 juice extractor (Mikachi model No 1706). The juice Digestible energy (kcal/kg) 2717.86 obtained was designated as soursop juice (SSJ) and kept Ether extract (%) 3.34 frozen 4 °C in disposable 5 ml sterile sample bottles until Crude fibre (%) 16.48 its required for use. Lysine (%) 1.01 Experimental animal and management Methionine (%) 0.75 Sixty (60) mixed breed (New Zealand white x Chinchilla) Calcium (%) 1.60 male rabbit bucks kept in a battery cage system kept in an Phosphorus (%) 0.45 open-sided house were used for the experiment. The Jimoh et al. Journal of Animal Science and Technology (2018) 60:28 Page 3 of 6 th control as non-heat stressed treatment. The fastened the overall mean for each character; B is the fixed effect of i −1 blood sample was collected at 28 days and 56 days of the Soursop (SSJ) was administered 5 levels (i=0.55 mlkg BW −1 −1 study. Blood was collected through the marginal ear vein water (control), 0.55 mlkg BW SSJ, 1.11 mlkg BW −1 −1 into a sample bottle. Serum was separated by centrifuga- SSJ, 1.67 mlkg BW SSJ and 2.22 mlkg BW SSJ); and tion (Medi Scan centrifuge model No 800D) and stored at e is the random residual effect. ijl -2 °C before analysis. Serum obtained was assayed for total protein, albumin, cholesterol, and triglyceride Results using commercial assay kits and its procedure, lipid Serum oxidative status of non-heat stressed treatment peroxidation, reduced glutathione, catalase, and super- is shown in Table 2. Total protein, antioxidant activities oxide dismutase activity using standard procedures. were higher than values obtained in heat stressed Superoxide dismutase (SOD); to 2.1 ml of 50 m M groups. However, cholesterol and lipid peroxidation butter, 0.02 ml of enzyme source and 0.86 ml of distilled were lower in non-heat stressed group compared with water. The reaction is initiated with 0.02 ml of 10 mM heat stressed groups. pyrogallol and change in absorbance monitored at 420 mm. One unit of SOD is defined as that amount of enzyme required to inhibit to auto-oxidation of pyrogal- Serum oxidative status of heat-stressed bucks gavaged lol by 50℅ in standard assay system of 3 ml. The spe- with soursop juice cific activity is expressed as unit /min/mg protein. Serum oxidative status of heat stressed bucks gavaged Catalase activity; the assay system contain 1.9 ml,0.05 M with soursop juice for 4 weeks is shown in Table 3.The buffer PH 7.0 and 1.0 ml 0.059 M water. The reaction is serum total protein of bucks on control were statistically initiated by addition of 0.1 ml enzyme source. The (p > 0.05) similar with bucks on treatments 3, 4 and 5. decrease in absorbance is monitored at 1 min interval Cholesterol of bucks on SSJ based treatments were for 5 min at 240 min and activity is expressed as moles significantly (p < 0.05) lower than those on treatment of water decomposed /min/mg protein. 1. Triglyceride declined with increased SSJ adminis- The assay for lipid peroxidation; The reaction mixture tration. Bucks on treatments 2, 3, 4 and 5 had signifi- in a total volume of 3.0 ml contained 1.0 ml serum, cantly (p < 0.05) low values while bucks not offered 1.0 ml of TCA (0.67%). All the test tubes were placed in SSJ had the statistically highest value. Serum lipid a boiling water bath for a period of 45 min. The tubes peroxidation was significantly (p < 0.05) highest in the were shifted to the ice bath and then centrifuged at buck on control and least in bucks offered treatments 4 2500 rpm for 10 min. The amount of malondialdehyde and 5. However, bucks on treatments 2 and 3 had statisti- (MDA) formed in each of the samples was assessed by cally (p > 0.05) similar lipid peroxidation values and were measuring the optical density of the supernatant at significantly (p < 0.05) higher than bucks on treatments 4 532 nm. and 5. Glutathione of bucks on treatments 4 and 5 was The glutathione (GSH) content; in which 1.0 ml of significantly (p < 0.05) highest across the treatments with PMS fraction (10%) was mixed with 1.0 ml of sulphosa- significantly least values obtained in bucks on treatments licylic acid (4%).The sample was incubated at 4 °C for at 1 and 2. Superoxide dismutase activity was highest statisti- least 1 h and then subjected to centrifugation at cally in bucks on treatment 5, with bucks on treatments 1 1200 rpm for 15 min at 4 °C. The assay mixture con- and 2 having the significantly (p < 0.05) least values. Bucks tained 0.4 ml filtered aliquot, 2.2 ml phosphate, buffer on treatment 3 and 4 had lower SOD than bucks on treat- (0.1 M, PH 7.4) and 0.4 ml DTNB (10 mM) in a total ment 5. Serum catalase activity in SSJ based groups was volume of 3.0 ml. The yellow colour developed was read significantly higher than the control. immediately at 412 mm. Table 2 baseline of serum oxidative status of the experimental rabbits at absence of heat stress Statistical analysis Parameters Baseline assessment Data obtained were subjected to analysis of variance at (un-heat stressed treatment) α = 0.05, the general linear model procedure of SAS, Total Protein (g/dL) 54.8 while means were separated using Duncan’s multiple Cholesterol (mg/dL) 51.04 range test of same software. Triglyceride (mg/dL) 114.53 The statistical model is as the following: Lipid Peroxidation (TBARS/mg protein) 0.09 Y ¼ μ þ B þ e ijl i ijl Glutathione (μg GSH /min/mg protein) 54.05 Catalase (nm H O /min/mg protein) 132.77 2 2 Where Y represents the value of serum biochemical pa- ijl Superoxide Dismutase (U/min/mg protein) 78.68 th rameters and oxidative status measured in the l animal; μ is Jimoh et al. Journal of Animal Science and Technology (2018) 60:28 Page 4 of 6 Table 3 Serum oxidative status of heat stressed bucks gavaged with soursop juice for 4 weeks Treatment 1 Treatment 2 Treatment 3 Treatment 4 Treatment 5 SEM − 1 − 1 − 1 − 1 −1 (0 mlkg BW) (0.55 mlkg BW) (1.11 mlkg BW) (1.67 mlkg BW) (2.22 mlkg BW) a b a a a Total Protein (g/dL) 54.8 14.92 8.57 14.28 13.18 11.10 1.24 a b b b b Cholesterol (mg/dL) 51.04 61.17 48.26 46.95 50.47 50.88 3.86 a b c c c Triglyceride (mg/dL) 114.53 148.01 129.61 103.49 103.31 99.52 9.09 a b b c c Lipid Peroxidation 0.09 1.46 0.90 0.96 0.79 0.75 0.05 (TBARS/mg protein) c c b a a Glutathione 54.05 17.39 20.90 27.08 33.86 38.46 3.48 (μg GSH /min/mg protein) b a a a a Catalase 132.77 54.01 95.05 87.38 90.02 96.50 6.38 (nm H O /min/mg protein) 2 2 c c b b a Superoxide Dismutase 78.68 21.74 24.64 35.87 38.26 60.63 3.62 (U/min/mg protein) Different superscipt denote statistically significant differences at p ≤ 0.05 Serum oxidative status of heat stressed bucks gavaged Discussion with soursop juice for 8 weeks (Table 4) reveal that Cholesterol and triglyceride values of SSJ drenched bucks serum total protein in bucks on treatments 3, 4 and 5 were lower than the control over 8 weeks. This shows that are statistically similar and significantly (p < 0.05) lower SSJ demonstrated the hypocholesterolemic effect in a than bucks on treatments 1 and 2. Serum cholesterol dose-dependent manner throughout the study, as evident of bucks on treatments 1, 2 and 3 are similar and in cholesterol and triglyceride values. This corroborates were statistically (p < 0.05) higher than bucks on treat- reports that A. muricata lowers hypertriglyceridemia and ment 4 and 5. Triglyceride of bucks on control was hypercholesterolemia in alloxan-induced diabetic rats [6]. significantly (p < 0.05) higher than bucks on SSJ based Zheng et al. [7] demonstrated that fruit and vegetable treatments. Serum lipid peroxidation of bucks on juice reduce total cholesterol in the body and improve treatment 1 was significantly (p < 0.05) highest, while cholesterol profile in the blood. The improving blood bucks on treatment 5 had significantly (p < 0.05) least lipids effects of the juice blend were attributed to the high values. Serum glutathione activity of bucks on SSJ content of total polyphenol. The trend of result shows that treatments were statistically similar and significantly total protein of SSJ drenched bucks was lower than (p < 0.05) higher than bucks on control. Serum cata- control and increase across the treatments with the period lase activity in SSJ based groups was significantly of administration. higher than the control. Superoxide dismutase activity SSJ reduced serum lipid peroxidation throughout the of bucks on treatment 1, 2, 3 and 4 was statistically study, this proves a beneficial effect of chronic adminis- similar and significantly (p < 0.05) lower than SOD of tration of SSJ on heat stressed bucks. This is revealed by buck on treatment 5. values of lipid peroxidation in SSJ drenched bucks, Table 4 Serum oxidative status of heat stressed bucks gavaged with soursop juice for 8 weeks Baseline assessment Treatment 1 Treatment 2 Treatment 3 Treatment 4 Treatment 5 SEM −1 −1 − 1 − 1 − 1 (un-heat stressed (0 mlkg BW) (0.55 mlkg BW) (1.11 mlkg BW) (1.67 mlkg BW) (2.22 mlkg BW) treatment) a a b b b Total Protein (g/dL) 54.8 43.39 39.20 32.70 29.60 24.15 2.27 a a a b b Cholesterol (mg/dL) 51.04 57.91 50.19 51.91 41.03 36.68 2.97 a b b b b Triglyceride (mg/dL) 114.53 214.78 134.15 177.05 155.75 129.77 10.89 a b b b c Lipid Peroxidation 0.09 1.41 0.35 0.38 0.29 0.19 0.04 (TBARS/mg protein) b a a a a Glutathione (μg GSH 54.05 27.79 37.28 38.01 45.31 45.99 4.29 /min/mg protein) b a a a a Catalase (nm H O 132.77 43.58 102.42 100.89 103.36 109.03 7.29 2 2 /min/mg protein) b b b b a Superoxide Dismutase 78.68 17.39 20.29 19.57 21.74 28.70 3.01 (U/min/mg protein) Different superscipt denote statistically significant differences at p ≤ 0.05 Jimoh et al. Journal of Animal Science and Technology (2018) 60:28 Page 5 of 6 which were lower at 8 weeks than at 4 weeks of the [11]. This study also agrees with the notion that study. This reveals that the duration of administration of antioxidant-rich juice/extracts are more effective when the SSJ enhanced mitigation of oxidant accumulations and/ body has undergone intense, long-term oxidative stress, or production in heat stressed bucks. Hypercholesterol- rather than in healthy individuals or in individuals under- emia is related to increased lipid peroxidation [7], thus going short-term or acute oxidative stress [11]. Zheng et the mechanism of soursop juice reduction of cholesterol al. [7] review antioxidant effects of several fruits and contributes to lowering lipid peroxidation as revealed in vegetable juice and concluded that the consumption of this work. Similarly, cranberry powder has been shown juice enhanced total antioxidant activity and enzymatic to decrease the accumulation of malondialdehyde antioxidants and are important therapies to ameliorate (MDA, an indicator of oxidative damage) in male New oxidative stress and its related diseases. Similarly, Syahida Zealand rabbit kidneys [8]. This is also supported by et al. [12]reportedthat Annona muricata L. extract claims that A. muricata extract has a protective and contains the high total antioxidant, which improved the beneficial effect on hepatic tissues subjected to STZ- total antioxidant status of Sprague-Dawley rats as the induced oxidative stress, by decreasing lipid peroxidation dosage increased, which is good in promoting health. and indirectly enhancing production of insulin and endogenous antioxidants [4]. Conclusion Glutathione activity in heat stressed bucks in- This study reveals that chronic oral administration of creased with the dosage of SSJ administration at soursop juice proved beneficial in promoting good 4 weeks. However, at 8 weeks though values were health of heat-stressed bucks. Soursop juice reduced higher than at 4 weeks, the effect of the accumula- serum lipid peroxidation and enhanced antioxidant tion of production of glutathione could account for activity in heat stressed rabbit over 8 weeks. Administra- their similar values in SSJ drenched groups. The tion of soursop juice to heat-stressed bucks at 2.22 −1 least values of glutathione were obtained in control mlkg BW offered optimum antioxidant defense against group throughout the study, this demonstrates the oxidative stress. enhancement of glutathione activity in heat stressed Abbreviations bucks by SSJ to counteract the accumulation of BW: Body weight; GSH: Glutathione; MDA: Malondialdehyde; ROS-M: Reactive hydrogen peroxide. This is also observed in catalase oxygen species and its metabolites; SAS: Statistical analysis software; SOD: Superoxide dismutase; SSJ: Soursop juice; THI: Temperature- activity of the bucks, catalase and glutathione are re- humidity index sponsible for the elimination of hydrogen peroxide in biological systems. Similarly, ginger also a natural anti- Acknowledgements The authors appreciate the Teaching and Research Farm, Department of oxidant spice has been reported to decrease lipid peroxi- Agricultural Technology, Federal Polytechnic, Ado-Ekiti, Nigeria, for making dation, increasing GSH content and maintaining normal available animals for the research. We are grateful to Kolawole Khadijah levels of antioxidant enzymes in rats [9]. Effect of chronic Abidemi and Abiola Saheed Olajide for the care and handling of the animals, and their resourcefulness to the study. antioxidant-rich fruit administration was also reported by Kota et al. [10] in rat supplemented ginger for one month, Funding which recorded significant increases in activity of antioxi- This research did not receive any specific grant from any funding agency in the public, commercial or not-for profit sector. dant enzymes (superoxide dismutase, glutathione peroxid- ase, and catalase) in the liver. Superoxide dismutase Availability of data and materials activity was higher at 4 weeks in SSJ drenched bucks than “The study was undertaken with approval from institutional ethics committee for care and use of animal for research of the Federal polytechnic Ado Ekiti.” at 8 weeks. This could be due to the first line defense of SOD to convert superoxide anion to hydrogen peroxide in Authors’ contributions heat stressed bucks at 4 weeks. After regulating super- JOA designed and supervised the study, carried out statistical analysis and wrote the first manuscript. AES co supervised the study and wrote the oxide anion production and elimination, SOD activity de- experimental layout. ASO and OIS carried out the field work, OWO clines to favour catalase and glutathione activity at the carried out the laboratory assay, ODO and DOT approved the experimental latter stage, to counteract the hydrogen peroxide being protocol, read and corrected the first manuscript. All authors read and approve the final manuscript. produced as a metabolite of SOD. It suggests that SOD functions in tandem with catalase and glutathione regulate Ethical approval superoxide anion and hydrogen peroxide productions This research was undertaken with approval from institutional ethics committee of the Department of Agricultural Technology, Federal and/or accumulation in the bucks. This result in mitigat- Polytechnic, Ado-Ekiti. The institutional and national standards for the care and ing oxidants (lipid peroxides) and prevent oxidative stress use of animals for research in the Research Policy Handbook of the Federal in heat stressed bucks. This demonstrates SSJ mechanism Polytechnic, Ado-Ekiti were followed and appropriate measures were taken to minimize pain or discomfort on the animals. to mitigate oxidative stress in heat stressed bucks. Contrariwise, cranberry and ginger had no effect on the Consent for publication oxidative stress or antioxidant status in exercising horses Not applicable. Jimoh et al. Journal of Animal Science and Technology (2018) 60:28 Page 6 of 6 Competing interests The authors declare that there are no competing interests to the publication of this article. Publisher’sNote Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations. Author details Department of Agricultural Technology, Federal Polytechnic Ado Ekiti, Ado Ekiti, Ekiti State, Nigeria. Department of Science Technology, Federal Polytechnic, Ado Ekiti, Ekiti State, Nigeria. Department of Animal Science, Adekunle Ajasin University Akungba Akoko, Akungba Akoko, Ondo State, Nigeria. Received: 25 September 2018 Accepted: 2 November 2018 References 1. Jimoh OA, Ewuola EO. Thermoregulatory response of exotic rabbit breeds during peak temperature humidity index of Ibadan. Tropical Animal Production investigation. 2016;19(1):41–7. 2. Jimoh OA, Ewuola EO, Balogun AS. Oxidative stress markers in exotic breeds of rabbit during peak of heat stress in Ibadan, Nigeria. Journal of Advances in Biology and Biotechnology. 2017;12(1):1–9. https://doi.org/10.9734/JABB/ 2017/30437. 3. Jimoh OA. Assessment of the oxidative stress markers and reproductive performance of four exotic breeds of rabbit in Ibadan. Ph.D. Thesis 2016, University of Ibadan, Ibadan, Nigeria. 4. Adewole SO,Ojewole JAO. Protective effects of Annona muricata linn. (annonaceae) leaf aqueous extract on serum lipid profiles and oxidative stress in hepatocytes of streptozotocin-treated diabetic rats. Afr. J. Traditional, Complementary and Alternative Medicines 2009, 6 (1): 30–41. 5. Marai IFM, Ayyat MS. Abd El-MonemUM. Growth performance and reproductive traits at first parity of New Zealand white female rabbits as affected by heat stress and its alleviation, under Egyptian conditions. Trop Anim Health Prod. 2001;33:1–12. 6. Sawant TP, Gogle DP. A brief review on recent advances in clinical research of Annona muricata. International journal of universal pharmacy and bio. Sciences. 2014;3(3):267–304. 7. Zheng J, Zhou Y, Li S, Zhang P, Zhou T, D X, Li H. Review effects and mechanisms of fruit and vegetable juices on cardiovascular diseases. Int J Mol Sci. 2017;18(555):1–15. https://doi.org/10.3390/ijms18030555. 8. Han CH, Kim SH, Kang SH, Shin OR, Lee HK, Kim HJ, Cho YH. Protective effects of cranberries on infected-induced oxidative renal damage in a rabbit model of vesico-ureteric reflux. BJU Int. 2007;100:1172–5. 9. Ahmed RS, Seth V, Pasha ST, Banerjee BD. Influence of dietary ginger (Zingiber Officinale Rosc) on oxidative stress induced by malathion in rats. Food Chem Toxicol. 2000;38:443–50. 10. Kota N, Krishna P, Polasa K. Alterations in antioxidant status of rats following intake of ginger through diet. Food Chem. 2008;106:991–6. 11. Smarsh DN, Liburt N, Streltsova J, Mckeever K, Williams CA. Oxidative stress and antioxidant status in intensely exercising horses administered nutraceutical extracts. Equine Vet J. 2010;42(Suppl. 38):317–22. https://doi. org/10.1111/j.2042-3306.2010.00182.x. 12. Syahida M, Maskat MY, Suri R, Mamot S, Hadijah H. Soursop (Annona muricata L.): blood hematology and serum biochemistry of Sprague-Dawley rats. Int Food Res J. 2012;19(3):955–9.

Journal

Journal of Animal Science and Technology – Springer Journals

Published: Nov 16, 2018

References

  • Thermoregulatory response of exotic rabbit breeds during peak temperature humidity index of Ibadan
    Jimoh, OA; Ewuola, EO
  • Oxidative stress markers in exotic breeds of rabbit during peak of heat stress in Ibadan, Nigeria
    Jimoh, OA; Ewuola, EO; Balogun, AS
  • Abd El-MonemUM. Growth performance and reproductive traits at first parity of New Zealand white female rabbits as affected by heat stress and its alleviation, under Egyptian conditions
    Marai, IFM; Ayyat, MS
  • A brief review on recent advances in clinical research of Annona muricata. International journal of universal pharmacy and bio
    Sawant, TP; Gogle, DP
  • Review effects and mechanisms of fruit and vegetable juices on cardiovascular diseases
    Zheng, J; Zhou, Y; Li, S; Zhang, P; Zhou, T; D, X; Li, H
  • Protective effects of cranberries on infected-induced oxidative renal damage in a rabbit model of vesico-ureteric reflux
    Han, CH; Kim, SH; Kang, SH; Shin, OR; Lee, HK; Kim, HJ; Cho, YH
  • Influence of dietary ginger (Zingiber Officinale Rosc) on oxidative stress induced by malathion in rats
    Ahmed, RS; Seth, V; Pasha, ST; Banerjee, BD
  • Alterations in antioxidant status of rats following intake of ginger through diet
    Kota, N; Krishna, P; Polasa, K
  • Oxidative stress and antioxidant status in intensely exercising horses administered nutraceutical extracts
    Smarsh, DN; Liburt, N; Streltsova, J; Mckeever, K; Williams, CA
  • Soursop (Annona muricata L.): blood hematology and serum biochemistry of Sprague-Dawley rats
    Syahida, M; Maskat, MY; Suri, R; Mamot, S; Hadijah, H