Comparative assessment of redox-sensitive biomarkers due to acacia honey and sodium arsenite administration in vivo

  • Oyeronke A. Odunola
  • Aliyu Muhammad
  • Ahsana D. Farooq
  • Kourosh Dalvandi
  • Huma Rasheed
  • Muhammad I. Choudhary
  • Ochuko L. Erukainure
Original Article


Apart from their nutritional properties, foods are basically health promoting or disease preventing. Typical example of such type of foods is honey. Sodium arsenite has been implicated in covalent interactions with the thiol groups in proteins, thereby affecting their structure–function relationship. This study was undertaken to investigate on the comparative assessment of redox-sensitive biomarkers from brain, blood serum and liver tissues as well as genotoxic effects in bone marrow cells of male Wister albino rats due to acacia honey and sodium arsenite administration in vivo. Male Wister albino in four groups of five rats, each were administered with distilled water, acacia honey (20 %), sodium arsenite (5 mg/kg body weight), acacia honey and sodium arsenite daily for 1 week. They were killed using 60 mg/kg sodium pentothal. Blood serum, brain and liver tissues were used for the assessment of GSH level, catalase, SOD activities, protein content and lipid peroxidation. The degree of clastogenicity was assessed using the mouse micronucleus assay in bone marrow cells. Sodium arsenite significantly (p < 0.05) suppresses the GSH level, SOD and catalase activities with simultaneous induction of lipid peroxidation (MDA) and clastogenic effects. Acacia honey was able to increased (p < 0.05) GSH level SOD and catalase activities with concomitant anti-clastogenic effects due to reduction in micronuclei. Acacia honey mitigates sodium arsenite induced-oxidative stress and clastogenicity in male Wister albino rats with its antioxidant properties more pronounced in liver tissues.


Acacia honey Sodium arsenite Oxidative stress Clastogenicity Wister albino rats 



This research work was partly supported by Education trust funds (ETF), Ahmadu Bello University Zaria, Nigeria, Muhammad Aliyu, P 20,348 and the facilities were provided by the Management of International Center for Chemical and Biological Sciences, University of Karachi, Karachi 75270, Pakistan towards the successful completion of this work.

Conflict of interest

The authors declared no conflict of interest.


  1. 1.
    Anklam E (1998) A review of the analytical methods to determine the geographical and Botanical origin of honey. Food Chem 63:549–562CrossRefGoogle Scholar
  2. 2.
    Gheldof N, Wang XH, Engeseth NJ (2002) Identification and quantification of antioxidant components of honeys from various floral sources. J Agric Food Chem 50:5870–5877CrossRefGoogle Scholar
  3. 3.
    Tchoumboue J, Awah-Ndukum J, Fonteh FA, Dongock ND, Pinta J, Movondo ZA (2007) Physico-chemical and microbiological characteristics of honey from the Sudano-Guinean zone of West Cameroon. Afr J Biotechnol 6:908–913Google Scholar
  4. 4.
    Hanaa MR, Shaymaa MMY (2011) Enhancement of the antitumor effect of honey and some of its extracts using adiponectin hormone. Aust J Basic Appl Sci 5(6):100–108Google Scholar
  5. 5.
    Fiorani Accorsi MA, Blasa M, Diamantini G, Piatti E (2006) Flavonoids from Italian multifloral honey reduce the extracellular ferricyanide in human red blood cells. J Agric Food Chem 54:8328–8334CrossRefGoogle Scholar
  6. 6.
    Alvarez-Suarez JM, Tulipani S, Romandini S, Bertoli E, Battino M (2010) Contribution of honey in nutrition and human health: a review. Med J Nutr Metab 3(1):15–23. doi: 10.1007/s12349-009-0051-6 CrossRefGoogle Scholar
  7. 7.
    Mohammadzadeh S, Sharriatpanahi M, Hamedi M, Amanzadeh Y, Ebrahimi SSE, Ostad SN (2007) Antioxidant power of Iranian propolis extract. Food Chem 103:729–733CrossRefGoogle Scholar
  8. 8.
    Muhammad A, Oyeronke AO, Solomon EO, Michael AG, Muhammad IC, Ahsana DF, Huma R, Ochuko LE, Shakil A (2012) Daily consumption of honey: effects on male Wister albino rats. Int J Food Nutr Saf 1(2):66–74CrossRefGoogle Scholar
  9. 9.
    Pichichero E, Cicconi R, Mattei M, Muzi MG, Canin A (2010) Acacia honey and chrysin reduce proliferation of melanoma cells through alterations in cell cycle progression. Int J Oncol 37:973–981Google Scholar
  10. 10.
    Alvarez-Suarez JM, Tulipani S, Diaz D, Estevez Y, Romandini S, Giampieri F, Damiani E, Astolfi P, Bompadre S, Battino M (2010) Antioxidant and antimicrobial capacity of several monofloral Cuban honeys and their correlation with color, polyphenol content and other chemical compounds. Food Chem Toxicol 48:2490–2499CrossRefGoogle Scholar
  11. 11.
    Alvarez-Suarez JM, González-Paramás AM, Santos-Buelga C, Battino M (2010) Antioxidant characterization of native monofloral Cuban honeys. J Agric Food Chem 58(17):9817–9824. doi: 10.1021/jf1018164 CrossRefGoogle Scholar
  12. 12.
    International Agency for Research on Cancer: Some Inorganic and Organometallic Compounds (1973) IARC monographs on the evaluation of carcinogenic risk of chemicals to humans, vol 2. International Agency for Research on Cancer, Lyon, France, p 181Google Scholar
  13. 13.
    Arteel GE, Luping G, Schlierf T (1981) Inorganic arsenic compounds. J Chem Soc Perkin Trans 1:2563Google Scholar
  14. 14.
    Chiou HY, Hsueh YM, Liaw KF (1995) Incidence of internal cancers and ingested inorganic arsenic: a seven-year follow-up study in Taiwan. Cancer Res 55:1296–1300Google Scholar
  15. 15.
    Smith A, Goycolea M, Haque R, Biggs ML (1998) Marked increase in bladder and Lung cancer mortality in a region of Northern Chile due to arsenic in drinking water. Am J Epidemiol 147:660–669CrossRefGoogle Scholar
  16. 16.
    Tsuda T, Babazono A, Yamamoto E, Kurumatini N, Mino Y, Ogawa T, Kishi Y, Aoyama H (1995) Ingested arsenic and internal cancer: a historical cohort study followed for 33 years. Am J Epidemiol 141:198–209Google Scholar
  17. 17.
    Odunola OA, Kazeem A, Akinwumi B (2007) Interaction and enhancement of the toxic effects of sodium arsenite and lead acetate in Wister rats. Afr J Biomed Res 10:59–65Google Scholar
  18. 18.
    Sharma A, Mukesh Kumar S, Madhu K (2009) Modulatory role of Emblica officinalis fruit extract against arsenic induced oxidative stress in Swiss albino mice. Chem Biol Interact 180(1):20–30CrossRefGoogle Scholar
  19. 19.
    Roy S, Roy M, Pandey PK, Tiwari SP (2009) Effects of tissue trace minerals status and histopathological changes in chronic. Arsenicosis in goats. Vet World 2(1):8–9Google Scholar
  20. 20.
    Srinivas SV, Arun PN (2007) Effect of arsenic and chromium on the serum amino-transferase activity in Indian major carp, Labeo rohita. Int J Environ Res Public Health 4(3):224–227CrossRefGoogle Scholar
  21. 21.
    Yu BP (1994) Cellular defense against damage from reactive oxygen species. Physiol Rev 74:139Google Scholar
  22. 22.
    Halliwell B, Gutteridge JMC (1988) In free radicals in biology and medicine, vol 1, 2nd edn. Clarendon Press, OxfordGoogle Scholar
  23. 23.
    Lata H, Ahuja GK (2003) Role of free radicals in health and diseases. Ind J Physio Allied Sci 57:124Google Scholar
  24. 24.
    Chowdhury P, Soulsby M (2002) Lipid peroxidation in rat brain is increased by simulated weightlessness and decreased by a soy-protein diet. Ann Clin Lab Sci 32(2):188–192Google Scholar
  25. 25.
    Aebi HE (1983) Methods in enzymatic analysis. Academic Press, New York, pp 273–302Google Scholar
  26. 26.
    Misra H, Fridovich I (1972) The role of superoxide anion in the autooxidation of epinephrine and a simple assay for superoxide dismutase. J Biol Chem 247:3170Google Scholar
  27. 27.
    Ellman G (1959) Tissue sulphydryl groups. Arch Biochem Biophys 32:70–77CrossRefGoogle Scholar
  28. 28.
    Heddle JA, Salmone MF (1981) The micronuclei assay: in vivo. In: Stich HF, San RHC (eds) Topics in environmental physiology and medicine. Short term tests for chemical carcinogens. Springer, New York, pp 243–249CrossRefGoogle Scholar
  29. 29.
    Heddle JA, Sudharsan RA, Krepinsky AB (1981) The micronucleus assay II: in vitro. In: Stich HF, San RHC (eds) Topics in environmental physiology and medicine. Short term tests for chemical carcinogens. Springer, New York, pp 250–254CrossRefGoogle Scholar
  30. 30.
    Niki E (2012) Antioxidant capacity: which capacity and how to assess it? J Berry Res 1(4):169–176. doi: 10.3233/JBR-2011-018 Google Scholar
  31. 31.
    Chiva-Blanch G, Visioli F (2012) Polyphenols and health: moving beyond antioxidants. J Berry Res 2(2):63–71. doi: 10.3233/JBR-2012-028 Google Scholar
  32. 32.
    Muhammad S, Amusa NA (2005) The important food crops and medicinal plants of north western Nigeria. Res J Agric Biol Sci 1:254–260Google Scholar
  33. 33.
    French VM, Cooper RM, Molan PC (2005) The antibacterial activity of honey against coagulase-negative staphylococci. J Antimicrob Chemother 56:228–231CrossRefGoogle Scholar
  34. 34.
    Winsk SI, Carter DE (1995) Interactions of rat red blood cell sulfhydryls with arsenate and arsenite. Toxicol Environ Health 46:379–397CrossRefGoogle Scholar
  35. 35.
    Ramos O, Carrizales L, Yarez L, Barriga F (1995) Arsenic increased lipid peroxidation in rats tissues by a mechanism independent of glutathione levels. Environ Health Perspect 103:85–88Google Scholar
  36. 36.
    Poli G, Leonarduzzi G, Biasi F, Chiarpotto E (2004) Oxidative stress and cell signaling. Curr Med Chem 11:1163–1182CrossRefGoogle Scholar
  37. 37.
    Bhattacharya S, Haldar PK (2012) Ameliorative effect Trichosanthes dioica root against experimentally induced arsenic toxicity in male albino rats. Environ Toxicol Pharmacol 33:394–402CrossRefGoogle Scholar
  38. 38.
    Guha Mazumder DN (2008) Chronic arsenic toxicity and human health. Ind J Med Res 128:436–447Google Scholar
  39. 39.
    Kapaj S, Peterson H, Liber K, Bhattacharya P (2006) Human health effects from chronic arsenic poisoning—a review. J Environ Sci Health A 41:2399–2428CrossRefGoogle Scholar
  40. 40.
    Omotayo OE, Sulaiman SA, Wahab MSA (2012) Honey: a novel antioxidant. Molecules 17:4400–4423CrossRefGoogle Scholar
  41. 41.
    Alvarez-Suarez JM, Giampieri F, Damiani E, Astolfi P, Fattorini D, Regoli F, Quiles JL, Battino M (2012) Radical-scavenging activity, protective effect against lipid peroxidation and mineral contents of monofloral Cuban honeys. Plant Foods Hum Nutr 67(1):31–38. doi: 10.1007/s11130-011-0268-7 CrossRefGoogle Scholar
  42. 42.
    Khalil MI, Alam N, Moniruzzaman M, Sulaiman SA, Gan SH (2011) Phenolic acid composition and antioxidant properties of Malaysian honeys. J Food Sci 76:921–928CrossRefGoogle Scholar
  43. 43.
    Van den Berg AJ, van den Worm E, van Ufford HC, Halkes SB, Hoekstra MJ, Beukelman CJ (2008) An in vitro examination of the antioxidant and anti-inflammatory properties of buckwheat honey. J Wound Care 17:172–178Google Scholar
  44. 44.
    Beretta G, Orioli M, Facino RM (2007) Antioxidant and radical scavenging activity of honey in endothelial cell cultures (EA.hy926). Planta Med 73:1182–1189CrossRefGoogle Scholar
  45. 45.
    Kishore RK, Halim AS, Syazana MS, Sirajudeen KN (2011) Tualang honey has higher phenolics content and greater radical scavenging activity compared with other honey sources. Nutr Res 31:322–325CrossRefGoogle Scholar
  46. 46.
    Marghitas LA, Dezmirean DS, Pocol CB, Ilea M, Bobis O, Gergen I (2010) The development of a biochemical profile of acacia honey by identifying biochemical determinants of its quality. Not Bot Hort Agrobot Cluj Special Issue 38(2):84–90Google Scholar
  47. 47.
    Alvarez-Suarez JM, Giampieri F, Gonzalez-Paramas AM, Damiani E, Astolfi P, Martinez-Sanchez G, Bompadre S, Quiles JL, Santos-Buelga C, Battino M (2012) Phenolics from monofloral honeys protect human erythrocyte membranes against oxidative damage. Food Chem Toxicol. doi: 10.1016/j.fct.2012.01.042 Google Scholar
  48. 48.
    Gharzouli K, Amira S, Gharzouli A, Khennouf S (2002) Gastroprotective effects of honey and glucose-fructose-sucrose-maltose mixture against ethanol-, indomethacin- and acidified aspirin-induced lesions in the rat. Exp Toxicol Pathol 54:217–221CrossRefGoogle Scholar
  49. 49.
    Al-Waili NS, Saloom KY, Al-Waili TN, Al-Waili AN, Akmal M, Al-Waili FS, Al-Waili HN (2006) Influence of various diet regimens on deterioration of hepatic function and hematological parameters following carbon tetrachloride: a potential protective role of natural honey. Nat Prod Res 20:1258–1264CrossRefGoogle Scholar
  50. 50.
    Mohamed M, Sulaiman SA, Jaafar H, Sirajudeen KN (2011) Effect of different doses of Malaysian honey on reproductive parameters in adult male rats. Andrologia. doi: 10.1111/j.1439-0272.2010.01159.x Google Scholar
  51. 51.
    Zaid SS, Sulaiman SA, Sirajudeen KN, Othman NH (2011) The effects of Tualang honey on female reproductive organs, tibia bone and hormonal profile in ovariectomised rats-animal model for menopause. BMC Complement Altern Med 10:82CrossRefGoogle Scholar
  52. 52.
    Erejuwa OO, Gurtu S, Sulaiman SA, Ab Wahab MS, Sirajudeen KN, Salleh MS (2010) Hypoglycemic and antioxidant effects of honey supplementation in streptozotocin-induced diabetic rats. Int J Vitam Nutr Res 80:74–82CrossRefGoogle Scholar
  53. 53.
    Kassim M, Achoui M, Mustafa MR, Mohd MA, Yusoff KM (2010) Ellagic acid, phenolic acids and flavonoids in Malaysian honey extracts demonstrate in vitro anti-inflammatory activity. Nutr Res 30:650–659CrossRefGoogle Scholar
  54. 54.
    Testoni ML, Bolzan AD, Bianchi NO (1997) Effects of antioxidants on streptonigrin-induced DNA damage and clastogenesis in CHO cells. Mutat Res 373(2):201–206CrossRefGoogle Scholar
  55. 55.
    Sunderman FW (1984) Recent advances in metal carcinogenesis. Ann Clin Lab Sci 14:93–122Google Scholar
  56. 56.
    Aliyu M, Odunola OA, Owumi SE, Habila N, Aimola IA, Ochuko LE (2012) Ethanol suppresses the effects of sodium arsenite in male Wister albino rats. 1:222. doi: 10.4172/scientificreports.222
  57. 57.
    Owumi SE, Odunola OA, Aliyu M (2012) Co-administration of sodium arsenite and ethanol: Protection by aqueous extract of Aframomum longiscapum seeds. Phcog Res 4:154–160CrossRefGoogle Scholar
  58. 58.
    Li JH, Rossman TG (1989) Inhibition of DNA ligase activity by arsenite: a possible mechanism of its co-mutagenesis. Mol Toxicol 2:1–9Google Scholar
  59. 59.
    Lasko DD, Tomkinson AE, Lindahl T (1990) Eukaryotic DNA ligases. Mutat Res 236:277–287CrossRefGoogle Scholar
  60. 60.
    Oyeronke AO, Adewale A, Olubukola SO, Olufunke O (2005) Protection against 2-acetyl aminofluorene induced toxicity in mice by garlic (Allium sativum), Bitter kola (Garcinia kola seed) and honey. Afr J Med Med Sci 34:167–172Google Scholar

Copyright information

© Springer-Verlag Italia 2013

Authors and Affiliations

  • Oyeronke A. Odunola
    • 1
  • Aliyu Muhammad
    • 1
    • 2
    • 3
  • Ahsana D. Farooq
    • 2
  • Kourosh Dalvandi
    • 3
  • Huma Rasheed
    • 3
  • Muhammad I. Choudhary
    • 2
    • 3
  • Ochuko L. Erukainure
    • 2
  1. 1.Department of BiochemistryUniversity of IbadanIbadanNigeria
  2. 2.H.E.J. Research Institute of Chemistry, International Center for Chemical and Biological SciencesUniversity of KarachiKarachiPakistan
  3. 3.Dr. Panjwani Center for Molecular Medicine and Drug Research, International Center for Chemical and Biological SciencesUniversity of KarachiKarachiPakistan

Personalised recommendations