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Evidence-Based Complementary and Alternative Medicine
Volume 2016 (2016), Article ID 7387286, 11 pages
http://dx.doi.org/10.1155/2016/7387286
Research Article

Unsweetened Natural Cocoa Powder Has the Potential to Attenuate High Dose Artemether-Lumefantrine-Induced Hepatotoxicity in Non-Malarious Guinea Pigs

1Department of Pharmacology and Toxicology, University of Ghana School of Pharmacy, College of Health Sciences, Legon, Ghana
2Department of Chemical Pathology, School of Biomedical and Allied Health Sciences, College of Health Sciences, Korle-Bu, Ghana
3Department of Physiology, School of Biomedical and Allied Health Sciences, College of Health Sciences, Korle-Bu, Ghana
4Department of Pharmaceutical Chemistry, University of Ghana School of Pharmacy, College of Health Sciences, Legon, Ghana
5Department of Animal Experimentation, Noguchi Memorial Institute for Medical Research, College of Health Sciences, Accra, Ghana

Received 29 March 2016; Revised 30 May 2016; Accepted 8 June 2016

Academic Editor: Mohamed M. Abdel-Daim

Copyright © 2016 Isaac Julius Asiedu-Gyekye et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. World Health Organisation, World Malaria Report, World Health Organisation, Geneva, Switzerland, 2012.
  2. World Health Organization, World Malaria Report, World Health Organization, Geneva, Switzerland, 2007.
  3. P. B. Bloland, M. Ettling, and S. Meek, “Combination therapy for malaria in Africa: hype or hope?” Bulletin of the World Health Organization, vol. 78, no. 12, pp. 1378–1388, 2000. View at Google Scholar · View at Scopus
  4. World Health Organization, Guidelines for the Treatment of Malaria, World Health Organisation (WHO), Geneva, Switzerland, 3rd edition, 2015.
  5. B. K. Brice, Y. William, O. Lacina et al., “In vitro susceptibility of Plasmodium falciparum isolates from Abidjan, Côte d'Ivoire, to artemisinin, chloroquine, dihydroartemisinin and pyronaridine,” Tanzania Journal of Health Research, vol. 12, no. 1, pp. 73–79, 2010. View at Google Scholar · View at Scopus
  6. World Health Organization, Antimalarial Drug Combination Therapy: Report of a Technical Consultation, World Health Organisation (WHO), Geneva, Switzerland, 2007.
  7. A. M. Dondorp, F. Nosten, P. Yi et al., “Artemisinin resistance in Plasmodium falciparum malaria,” The New England Journal of Medicine, vol. 361, no. 5, pp. 455–467, 2009. View at Publisher · View at Google Scholar · View at Scopus
  8. A. P. Phyo, S. Nkhoma, K. Stepniewska et al., “Emergence of artemisinin-resistant malaria on the western border of Thailand: a longitudinal study,” The Lancet, vol. 379, no. 9830, pp. 1960–1966, 2012. View at Publisher · View at Google Scholar · View at Scopus
  9. S. E. Owumi, M. A. Gbadegesin, O. A. Odunola, A. M. Adegoke, and A. O. Uwaifo, “Toxicity associated with repeated administration of artemether-lumefantrine in rats,” Environmental Toxicology, vol. 30, no. 3, pp. 301–307, 2015. View at Publisher · View at Google Scholar · View at Scopus
  10. Worldwide Antimalarial Resistance Network (WWARN) AL Dose Impact Study Group, “The effect of dose on the antimalarial efficacy of artemether-lumefantrine: a systematic review and pooled analysis of individual patient data,” The Lancet Infectious Diseases, vol. 15, no. 6, pp. 692–702, 2015. View at Publisher · View at Google Scholar
  11. M. J. A. Maleyki and A. Ismail, “Antioxidant properties of cocoa powder,” Journal of Food Biochemistry, vol. 34, no. 1, pp. 111–128, 2010. View at Publisher · View at Google Scholar · View at Scopus
  12. A. H. Azizah, N. M. Nik Ruslawati, and T. Swee Tee, “Extraction and characterization of antioxidant from cocoa by-products,” Food Chemistry, vol. 64, no. 2, pp. 199–202, 1999. View at Publisher · View at Google Scholar · View at Scopus
  13. M. Karim, K. McCormick, and C. Tissa Kappagoda, “Effects of cocoa extracts on endothelium-dependent relaxation,” The Journal of Nutrition, vol. 130, no. 8, pp. 2105S–2108S, 2000. View at Google Scholar · View at Scopus
  14. L. Stahl, K. B. Miller, J. Apgar et al., “Preservation of cocoa antioxidant activity, total polyphenols, flavan-3-ols, and procyanidin content in foods prepared with cocoa powder,” Journal of Food Science, vol. 74, no. 6, pp. C456–C461, 2009. View at Publisher · View at Google Scholar · View at Scopus
  15. I. Amin, B. Koh, and R. Asmah, “Effect of cacao liquor on tumor marker enzymes 492 during chemical hepatocarcinogenesis in rats,” Journal of Medicinal Food, vol. 7, no. 1, pp. 7–12, 2004. View at Publisher · View at Google Scholar
  16. I. Cordero-Herrera, M. A. Martín, L. Goya, and S. Ramos, “Cocoa flavonoids protect hepatic cells against high-glucose-induced oxidative stress: relevance of MAPKs,” Molecular Nutrition and Food Research, vol. 59, no. 4, pp. 597–609, 2015. View at Publisher · View at Google Scholar · View at Scopus
  17. S. K. Amponsah, K. A. Bugyei, D. Osei-Safo et al., “In vitro activity of extract and fractions of natural cocoa powder on Plasmodium falciparum,” Journal of Medicinal Food, vol. 15, no. 5, pp. 476–482, 2012. View at Publisher · View at Google Scholar · View at Scopus
  18. F. K. Addai, “Natural cocoa as diet-mediated antimalarial prophylaxis,” Medical Hypotheses, vol. 74, no. 5, pp. 825–830, 2010. View at Publisher · View at Google Scholar · View at Scopus
  19. C. Andres-Lacueva, M. Monagas, N. Khan et al., “Flavanol and flavonol contents of cocoa powder products: influence of the manufacturing process,” Journal of Agricultural and Food Chemistry, vol. 56, no. 9, pp. 3111–3117, 2008. View at Publisher · View at Google Scholar · View at Scopus
  20. A. Caligiani, D. Acquotti, M. Cirlini, and G. Palla, “1H NMR study of fermented cocoa (Theobroma cacao L.) beans,” Journal of Agricultural and Food Chemistry, vol. 58, no. 23, pp. 12105–12111, 2010. View at Publisher · View at Google Scholar · View at Scopus
  21. M. Del Rosario Brunetto, L. Gutiérrez, Y. Delgado et al., “Determination of theobromine, theophylline and caffeine in cocoa samples by a high-performance liquid chromatographic method with on-line sample cleanup in a switching-column system,” Food Chemistry, vol. 100, no. 2, pp. 459–467, 2007. View at Publisher · View at Google Scholar · View at Scopus
  22. L. Tian, X. Shi, L. Yu, J. Zhu, R. Ma, and X. Yang, “Chemical composition and hepatoprotective effects of polyphenol-rich extract from houttuynia cordata tea,” Journal of Agricultural and Food Chemistry, vol. 60, no. 18, pp. 4641–4648, 2012. View at Publisher · View at Google Scholar · View at Scopus
  23. H. Shimoda, J. Tanaka, M. Kikuchi et al., “Walnut polyphenols prevent liver damage induced by carbon tetrachloride and d-galactosamine: hepatoprotective hydrolyzable tannins in the kernel pellicles of walnut,” Journal of Agricultural and Food Chemistry, vol. 56, no. 12, pp. 4444–4449, 2008. View at Publisher · View at Google Scholar · View at Scopus
  24. J. Yang, Y. Li, F. Wang, and C. Wu, “Hepatoprotective effects of apple polyphenols on CCl4-induced acute liver damage in mice,” Journal of Agricultural and Food Chemistry, vol. 58, no. 10, pp. 6525–6531, 2010. View at Publisher · View at Google Scholar · View at Scopus
  25. S. M. Sabir, S. D. Ahmad, A. Hamid et al., “Antioxidant and hepatoprotective activity of ethanolic extract of leaves of Solidago microglossa containing polyphenolic compounds,” Food Chemistry, vol. 131, no. 3, pp. 741–747, 2012. View at Publisher · View at Google Scholar · View at Scopus
  26. T. I. Stark, H. Justus, and T. Hofmann, “Quantitative analysis of N-phenylpropenoyl-l-amino acids in roasted coffee and cocoa powder by means of a stable isotope dilution assay,” Journal of Agricultural and Food Chemistry, vol. 54, no. 8, pp. 2859–2867, 2006. View at Publisher · View at Google Scholar · View at Scopus
  27. T. Adzet, J. Camarasa, and J. C. Laguna, “Hepatoprotective activity of polyphenolic compounds from Cynara scolymus against CCl4 toxicity in isolated rat hepatocytes,” Journal of Natural Products, vol. 50, no. 4, pp. 612–617, 1987. View at Publisher · View at Google Scholar · View at Scopus
  28. T. Rassaf and M. Kelm, “Cocoa flavanols and the nitric oxide-pathway: targeting endothelial dysfunction by dietary intervention,” Drug Discovery Today: Disease Mechanisms, vol. 5, no. 3-4, pp. e273–e278, 2008. View at Publisher · View at Google Scholar · View at Scopus
  29. W. M. Hon, K. H. Lee, and H. E. Khoo, “Nitric oxide in liver diseases: friend, foe, or just passerby?” Annals of the New York Academy of Sciences, vol. 962, pp. 275–295, 2002. View at Publisher · View at Google Scholar · View at Scopus
  30. Y. Li, D.-M. Zhang, J.-B. Li, S.-S. Yu, Y. Li, and Y.-M. Luo, “Hepatoprotective sesquiterpene glycosides from sarcandra glabra,” Journal of Natural Products, vol. 69, no. 4, pp. 616–620, 2006. View at Publisher · View at Google Scholar · View at Scopus
  31. M. Yoshikawa, T. Morikawa, Y. Kashima, K. Ninomiya, and H. Matsuda, “Structures of new dammarane-type triterpene saponins from the flower buds of Panax n otoginseng and hepatoprotective effects of principal ginseng saponins 1,” Journal of Natural Products, vol. 66, no. 7, pp. 922–927, 2003. View at Publisher · View at Google Scholar
  32. E. A. Adewusi and A. J. Afolayan, “A review of natural products with hepatoprotective activity,” Journal of Medicinal Plants Research, vol. 4, no. 13, pp. 1318–1334, 2010. View at Google Scholar · View at Scopus
  33. Y. Wu, F. Wang, Q. Zheng et al., “Hepatoprotective effect of total flavonoids from Laggera alata against carbon tetrachloride-induced injury in primary cultured neonatal rat hepatocytes and in rats with hepatic damage,” Journal of Biomedical Science, vol. 13, no. 4, pp. 569–578, 2006. View at Publisher · View at Google Scholar · View at Scopus
  34. A. J. Mungole, R. Awati, A. Chaturvedi, and P. Zanwar, “Preliminary phytochemical screening of Ipomoea obscura (L)—a hepatoprotective medicinal plant,” International Journal of PharmTech Research, vol. 2, no. 4, pp. 2307–2312, 2010. View at Google Scholar · View at Scopus
  35. E. Ronen, “Micro-elements in agriculture,” Practical Hydroponics and Greenhouses, pp. 39–48, 2007. View at Google Scholar
  36. World Health Organization, Quality Control Methods for Medicinal Plant Materials, WHO Offset, Geneva, Switzerland, 1998.
  37. E. H. Jihen, M. Imed, H. Fatima, and K. Abdelhamid, “Protective effects of selenium (Se) and zinc (Zn) on cadmium (Cd) toxicity in the liver and kidney of the rat: histology and Cd accumulation,” Food and Chemical Toxicology, vol. 46, no. 11, pp. 3522–3527, 2008. View at Publisher · View at Google Scholar · View at Scopus
  38. I. Messaoudi, J. El Heni, F. Hammouda, K. Saïd, and A. Kerkeni, “Protective effects of selenium, zinc, or their combination on cadmium-induced oxidative stress in rat kidney,” Biological Trace Element Research, vol. 130, no. 2, pp. 152–161, 2009. View at Publisher · View at Google Scholar · View at Scopus
  39. M. J. Anjos, R. T. Lopes, E. F. O. Jesus, S. M. Simabuco, and R. Cesareo, “Quantitative determination of metals in radish using X-ray fluorescence spectrometry,” X-Ray Spectrometry, vol. 31, no. 2, pp. 120–123, 2002. View at Publisher · View at Google Scholar · View at Scopus
  40. J. B. Harborne, Phytochemical Methods: A Guide to Modern Techniques of Plant Analysis, Chapman & Hall, London, UK, 1998.
  41. Z. Krastev, “Liver Damage Score—a new index for evaluation of the severity of chronic liver diseases,” Hepato-Gastroenterology, vol. 45, no. 19, pp. 160–169, 1998. View at Google Scholar · View at Scopus
  42. P. Alavinejad, F. Farsi, A. Rezazadeh et al., “The effects of dark chocolate consumption on lipid profile, fasting blood sugar, liver enzymes, inflammation, and antioxidant status in patients with non-alcoholic fatty liver disease: a randomized, placebo-controlled, pilot study,” Journal of Gastroenterology and Hepatology Research, vol. 4, no. 12, pp. 1858–1864, 2015. View at Publisher · View at Google Scholar
  43. E. T. Olayinka and A. Ore, “Alterations in antioxidant status and biochemical indices following administration of dihydroartemisinin-piperaquine phosphate (p-ALAXIN®),” IOSR Journal of Pharmacy and Biological Sciences, vol. 5, no. 4, pp. 43–53, 2013. View at Publisher · View at Google Scholar
  44. N. Mumoli, M. Cei, and A. Cosimi, “Drug-related hepatotoxicity,” The New England Journal of Medicine, vol. 354, no. 20, pp. 2192–2193, 2006. View at Google Scholar · View at Scopus
  45. C. U. Ugokwe, H. C. Asomba, and I. O. Onwuzulike, “Hepatotoxicity potential of coartemether on wistar albino rat using liver enzyme assay,” Journal of Pharmacy and Biological Sciences, vol. 10, pp. 66–70, 2015. View at Google Scholar
  46. A. A. Ngokere, T. C. Ngokere, and A. P. Ikwudinma, “Acute study of histomorphological and biochemedical changes caused by artesunate in visceral organs of the rabbit,” Journal of Experimental and Clinical Anatomy, vol. 3, no. 4, pp. 11–16, 2004. View at Google Scholar
  47. A. Udobre, E. J. Edoho, O. Esevin, and E. I. Etim, “Effect of artemisinin with folic acid on the activities of aspartate amino transferase, alanine amino transferase and alkaline phosphatase in rat,” Asian Journal of Biochemistry, vol. 4, no. 2, pp. 55–59, 2009. View at Publisher · View at Google Scholar · View at Scopus
  48. O. A. Adaramoye, D. O. Osaimoje, A. M. Akinsanya, C. M. Nneji, M. A. Fafunso, and O. G. Ademowo, “Changes in antioxidant status and biochemical indices after acute administration of artemether, artemether-lumefantrine and halofantrine in rats,” Basic and Clinical Pharmacology and Toxicology, vol. 102, no. 4, pp. 412–418, 2008. View at Publisher · View at Google Scholar · View at Scopus
  49. A. S. Adekunle, C. O. Falade, E. O. Agbedana, and A. Egbe, “Assessment of side-effects of administration of artemether in humans,” Biology and Medicine, vol. 1, no. 3, pp. 15–19, 2009. View at Google Scholar · View at Scopus
  50. H. U. Nwanjo and G. Oze, “Acute hepatotoxicity following administration of artesunate in Guinea pigs,” The Internet Journal of Toxicology, vol. 4, no. 1, pp. 1–2, 2007. View at Google Scholar
  51. A. Ismail, Z. M. Marjan, and C. W. Foong, “Total antioxidant activity and phenolic content in selected vegetables,” Food Chemistry, vol. 87, no. 4, pp. 581–586, 2004. View at Publisher · View at Google Scholar · View at Scopus
  52. R. M. Lamuela-Raventós, A. I. Romero-Pérez, C. Andrés-Lacueva, and A. Tornero, “Review: health effects of cocoa flavonoids,” Food Science and Technology International, vol. 11, no. 3, pp. 159–176, 2005. View at Publisher · View at Google Scholar · View at Scopus
  53. A. B. Granado-Serrano, M. A. Martín, L. Bravo, L. Goya, and S. Ramos, “A diet rich in cocoa attenuates N-nitrosodiethylamine-induced liver injury in rats,” Food and Chemical Toxicology, vol. 47, no. 10, pp. 2499–2506, 2009. View at Publisher · View at Google Scholar · View at Scopus
  54. M. A. Martín, S. Ramos, R. Mateos et al., “Protection of human HepG2 cells against oxidative stress by cocoa phenolic extract,” Journal of Agricultural and Food Chemistry, vol. 56, no. 17, pp. 7765–7772, 2008. View at Publisher · View at Google Scholar · View at Scopus
  55. M. Natsume, N. Osakabe, M. Yamagishi et al., “Analyses of polyphenols in cacao liquor, cocoa, and chocolate by normal-phase and reversed-phase HPLC,” Bioscience, Biotechnology and Biochemistry, vol. 64, no. 12, pp. 2581–2587, 2000. View at Publisher · View at Google Scholar · View at Scopus
  56. M. Yamagishi, M. Natsume, A. Nagaki et al., “Antimutagenic activity of cacao: inhibitory effect of cacao liquor polyphenols on the mutagenic action of heterocyclic amines,” Journal of Agricultural and Food Chemistry, vol. 48, no. 10, pp. 5074–5078, 2000. View at Publisher · View at Google Scholar · View at Scopus
  57. M. Yamagishi, M. Natsume, N. Osakabe et al., “Effects of cacao liquor proanthocyanidins on PhIP-induced mutagenesis in vitro, and in vivo mammary and pancreatic tumorigenesis in female Sprague-Dawley rats,” Cancer Letters, vol. 185, no. 2, pp. 123–130, 2002. View at Publisher · View at Google Scholar · View at Scopus
  58. Health Effects of Excess Copper; Copper in Drinking Water, The National Academies Press, Washington, DC, USA, 2000.
  59. E. Aidoo, F. K. Addai, J. Ahenkorah et al., “Natural cocoa ingestion reduced liver damage in mice infected with Plasmodium berghei (NK65),” Research and Reports in Tropical Medicine, vol. 3, pp. 107–116, 2012. View at Google Scholar
  60. G. Sokpor, F. K. Addai, R. K. Gyasi et al., “Voluntary ingestion of natural cocoa extenuated hepatic damage in rats with experimentally induced chronic alcoholic toxicity,” Functional Foods in Health and Disease, vol. 2, no. 5, pp. 166–187, 2012. View at Google Scholar
  61. K. Suzuki, K. Nakagawa, T. Yamamoto et al., “Carbon tetrachloride-induced hepatic and renal damages in rat: Inhibitory effects of cacao polyphenol,” Bioscience, Biotechnology and Biochemistry, vol. 79, no. 10, pp. 1669–1675, 2015. View at Publisher · View at Google Scholar · View at Scopus
  62. D. Taubert, R. Roesen, C. Lehmann, N. Jung, and E. Schömig, “Effects of low habitual cocoa intake on blood pressure and bioactive nitric oxide: a randomized controlled trial,” The Journal of the American Medical Association, vol. 298, no. 1, pp. 49–60, 2007. View at Publisher · View at Google Scholar · View at Scopus
  63. G. J. Dusting and P. S. Macdonald, “Endogenous nitric oxide in cardiovascular disease and transplantation,” Annals of Medicine, vol. 27, no. 3, pp. 395–406, 1995. View at Publisher · View at Google Scholar · View at Scopus
  64. S. Reagan-Shaw, M. Nihal, and N. Ahmad, “Dose translation from animal to human studies revisited,” The FASEB Journal, vol. 22, no. 3, pp. 659–661, 2008. View at Publisher · View at Google Scholar · View at Scopus