Table of Contents Author Guidelines Submit a Manuscript
Oxidative Medicine and Cellular Longevity
Volume 2018, Article ID 1780956, 10 pages
https://doi.org/10.1155/2018/1780956
Research Article

Anti-Inflammatory, Immunomodulatory, and Antioxidant Activities of Allicin, Norfloxacin, or Their Combination against Pasteurella multocida Infection in Male New Zealand Rabbits

1Department of Clinical Pathology, Faculty of Veterinary Medicine, Zagazig University, Zagazig, 44511 Sharkia, Egypt
2Department of Internal Medicine (Infectious Diseases), Faculty of Veterinary Medicine, Zagazig University, Zagazig, 44511 Sharkia, Egypt
3Biochemistry Department, Faculty of Science-Al Faisaliah, King Abdulaziz University, Jeddah, Saudi Arabia
4Bourgogne Franche-Comté University, Chrono-Environnement Laboratory, UMR CNRS 6249, 25030 Besançon Cedex, France
5Department of Pharmacology, Faculty of Veterinary Medicine, Suez Canal University, Ismailia 41522, Egypt

Correspondence should be addressed to Mohamed M. Abdel-Daim; ge.ude.zeus.tev@m.miadledba

Received 15 February 2018; Accepted 8 April 2018; Published 27 June 2018

Academic Editor: Mansur A. Sandhu

Copyright © 2018 Rasha T. M. Alam 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. F. Dziva, A. P. Muhairwa, M. Bisgaard, and H. Christensen, “Diagnostic and typing options for investigating diseases associated with Pasteurella multocida,” Veterinary Microbiology, vol. 128, no. 1-2, pp. 1–22, 2008. View at Publisher · View at Google Scholar · View at Scopus
  2. G. P. Langan, J. J. Lohmiller, S. P. Swing, and C. L. Wardrip, “Respiratory diseases of rodents and rabbits,” Veterinary Clinics of North America: Small Animal Practice, vol. 30, no. 6, pp. 1309–1335, 2000. View at Publisher · View at Google Scholar · View at Scopus
  3. S. Sanchez, S. Mizan, C. Quist et al., “Serological response to Pasteurella multocida NanH sialidase in persistently colonized rabbits,” Clinical and Vaccine Immunology, vol. 11, no. 5, pp. 825–834, 2004. View at Publisher · View at Google Scholar · View at Scopus
  4. P. B. Fernandes, “Mode of action, and in vitro and in vivo activities of the fluoroquinolones,” The Journal of Clinical Pharmacology, vol. 28, no. 2, pp. 156–168, 1988. View at Publisher · View at Google Scholar · View at Scopus
  5. M. P. Wentland, “Structure-activity relationships of fluoroquinolones,” The New Generation of Quinolones, pp. 1–43, 1990. View at Google Scholar
  6. T. A. Ahmad, S. S. Rammah, S. A. Sheweita, M. Haroun, and L. H. El-Sayed, “Development of immunization trials against Pasteurella multocida,” Vaccine, vol. 32, no. 8, pp. 909–917, 2014. View at Publisher · View at Google Scholar · View at Scopus
  7. P. Martino and F. Luzi, Bacterial Infections in Rabbit as Companion Animal: A Survey of Diagnostic Samples in Italy, 9th World Rabbit Congress, Verona-Italy, 2008.
  8. M. K. Fann and D. O'Rourke, “Normal bacterial flora of the rabbit gastrointestinal tract: a clinical approach,” Seminars in Avian and Exotic Pet Medicine, vol. 10, no. 1, pp. 45–47, 2001. View at Publisher · View at Google Scholar
  9. T. H. Abdullah, O. Kandil, A. Elkadi, and J. Carter, “Garlic revisited: therapeutic for the major diseases of our times?” Journal of the National Medical Association, vol. 80, no. 4, pp. 439–445, 1988. View at Google Scholar
  10. S. K. Banerjee, P. K. Mukherjee, and S. K. Maulik, “Garlic as an antioxidant: the good, the bad and the ugly,” Phytotherapy Research, vol. 17, no. 2, pp. 97–106, 2003. View at Publisher · View at Google Scholar · View at Scopus
  11. M. S. Butt, M. T. Sultan, M. S. Butt, and J. Iqbal, “Garlic: nature’s protection against physiological threats,” Critical Reviews in Food Science and Nutrition, vol. 49, no. 6, pp. 538–551, 2009. View at Publisher · View at Google Scholar · View at Scopus
  12. E. H. Abu Zeid, R. T. M. Alam, and N. E. Abd El-Hameed, “Impact of titanium dioxide on androgen receptors, seminal vesicles and thyroid hormones of male rats: possible protective trial with aged garlic extract,” Andrologia, vol. 49, no. 5, 2017. View at Publisher · View at Google Scholar · View at Scopus
  13. M. M. Abdel-Daim, N. K. M. Abdelkhalek, and A. M. Hassan, “Antagonistic activity of dietary allicin against deltamethrin-induced oxidative damage in freshwater Nile tilapia; Oreochromis niloticus,” Ecotoxicology and Environmental Safety, vol. 111, pp. 146–152, 2015. View at Publisher · View at Google Scholar · View at Scopus
  14. M. M. Abdel-Daim, O. E. Kilany, H. A. Khalifa, and A. A. M. Ahmed, “Allicin ameliorates doxorubicin-induced cardiotoxicity in rats via suppression of oxidative stress, inflammation and apoptosis,” Cancer Chemotherapy and Pharmacology, vol. 80, no. 4, pp. 745–753, 2017. View at Publisher · View at Google Scholar · View at Scopus
  15. S. Katoch, L. Verma, M. Sharma et al., “Experimental study of the pathogenicity of pasteurella multocida capsular type B in rabbits,” Journal of Comparative Pathology, vol. 153, no. 2-3, pp. 160–166, 2015. View at Publisher · View at Google Scholar · View at Scopus
  16. X.-H. Li, C.-Y. Li, Z.-G. Xiang et al., “Allicin ameliorates cardiac hypertrophy and fibrosis through enhancing of Nrf2 antioxidant signaling pathways,” Cardiovascular Drugs and Therapy, vol. 26, no. 6, pp. 457–465, 2012. View at Publisher · View at Google Scholar · View at Scopus
  17. B. Pavithra, N. Prakash, and K. Jayakumar, “PK-PD modelling of norfloxacin after oral administration in rabbits,” Veterinary World, vol. 3, no. 12, pp. 546–548, 2010. View at Google Scholar
  18. P. C. Wilkinson, Technique in Clinical Immunology, R. A. Thompson, Ed., Publication, USA, 1977.
  19. M. I. Muniz-Junqueira, C. E. Tosta, and A. Prata, “Phagocytic and bactericidal function of mouse macrophages to Salmonella typhimurium in schistosomiasis mansoni,” The American Journal of Tropical Medicine and Hygiene, vol. 46, no. 2, pp. 132–136, 1992. View at Publisher · View at Google Scholar · View at Scopus
  20. E. H. Coles, Veterinary Clinical Pathology: Saunders, W.B. Saunders Company, Philadelphia, PA, USA, 4th edition, 1986.
  21. S. Reitman and S. Frankel, “A colorimetric method for the determination of serum glutamic oxalacetic and glutamic pyruvic transaminases,” American Journal of Clinical Pathology, vol. 28, no. 1, pp. 56–63, 1957. View at Publisher · View at Google Scholar
  22. N. W. Tietz, Clinical Guide to Laboratory Tests, W. B. Saunders, Philadelphia, PA, USA, 3rd edition, 1995.
  23. S. Buhl and K. Jackson, “Optimal conditions and comparison of lactate dehydrogenase catalysis of the lactate-to-pyruvate and pyruvate-to-lactate reactions in human serum at 25, 30, and 37 degrees C,” Clinical Chemistry, vol. 24, no. 5, pp. 828–831, 1978. View at Google Scholar
  24. B. T. Doumas, D. D. Bayse, R. J. Carter, T. Peters Jr, and R. Schaffer, “A candidate reference method for determination of total protein in serum. I. Development and validation,” Clinical Chemistry, vol. 27, no. 10, pp. 1642–1650, 1981. View at Google Scholar
  25. F. Drupt, “Colorimetric determination of albumin,” Pharmaceutical Biology, vol. 9, p. 777, 1974. View at Google Scholar
  26. B. B. H. Doumas, “Determination of serumglobulin,” in Standard Methods of Clinical Chemistry, Academic Press, New York, 7th edition, 1972. View at Google Scholar
  27. D. J. Jollow, J. R. Mitchell, N. Zampaglione, and J. R. Gillette, “Bromobenzene-induced liver necrosis. Protective role of glutathione and evidence for 3, 4-bromobenzene oxide as the hepatotoxic metabolite,” Pharmacology, vol. 11, no. 3, pp. 151–169, 1974. View at Publisher · View at Google Scholar · View at Scopus
  28. M. Nishikimi, N. Appaji Rao, and K. Yagi, “The occurrence of superoxide anion in the reaction of reduced phenazine methosulfate and molecular oxygen,” Biochemical and Biophysical Research Communications, vol. 46, no. 2, pp. 849–854, 1972. View at Publisher · View at Google Scholar · View at Scopus
  29. H. Ohkawa, N. Ohishi, and K. Yagi, “Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction,” Analytical Biochemistry, vol. 95, no. 2, pp. 351–358, 1979. View at Publisher · View at Google Scholar · View at Scopus
  30. K. S. Suvarna, C. Layton, and J. D. Bancroft, Bancroft’s Theory and Practice of Histological Techniques E-Book: Elsevier Health Sciences, Elsevier Health Sciences, Churchill Livingstone, Australia, 7th edition, 2012.
  31. R. F. DiGiacomo, B. J. Deeb, W. E. Giddens Jr, B. L. Bernard, and M. M. Chengappa, “Atrophic rhinitis in New Zealand white rabbits infected with Pasteurella multocida,” American Journal of Veterinary Research, vol. 50, no. 9, pp. 1460–1465, 1989. View at Google Scholar
  32. T. Zimmerman, B. Deeb, and R. DiGiacomo, “Polypeptides associated with Pasteurella multocida infection in rabbits,” American Journal of Veterinary Research, vol. 53, no. 7, pp. 1108–1112, 1992. View at Google Scholar
  33. O. Palócz, J. Gál, P. Clayton et al., “Alternative treatment of serious and mild Pasteurella multocida infection in New Zealand White rabbits,” BMC Veterinary Research, vol. 10, no. 1, p. 276, 2014. View at Publisher · View at Google Scholar · View at Scopus
  34. S. Ankri and D. Mirelman, “Antimicrobial properties of allicin from garlic,” Microbes and Infection, vol. 1, no. 2, pp. 125–129, 1999. View at Publisher · View at Google Scholar · View at Scopus
  35. M. A. Dkhil, A. S. Abdel-Baki, F. Wunderlich, H. Sies, and S. Al-Quraishy, “Anticoccidial and antiinflammatory activity of garlic in murine Eimeria papillata infections,” Veterinary Parasitology, vol. 175, no. 1-2, pp. 66–72, 2011. View at Publisher · View at Google Scholar · View at Scopus
  36. S. Ankri, T. Miron, A. Rabinkov, M. Wilchek, and D. Mirelman, “Allicin from garlic strongly inhibits cysteine proteinases and cytopathic effects of Entamoeba histolytica,” Antimicrobial Agents and Chemotherapy, vol. 41, no. 10, pp. 2286–2288, 1997. View at Google Scholar
  37. A. Coppi, M. Cabinian, D. Mirelman, and P. Sinnis, “Antimalarial activity of allicin, a biologically active compound from garlic cloves,” Antimicrobial Agents and Chemotherapy, vol. 50, no. 5, pp. 1731–1737, 2006. View at Publisher · View at Google Scholar · View at Scopus
  38. S. R. Norrby and M. Jonsson, “Antibacterial activity of norfloxacin,” Antimicrobial Agents and Chemotherapy, vol. 23, no. 1, pp. 15–18, 1983. View at Publisher · View at Google Scholar · View at Scopus
  39. J. S. Wolfson and D. C. Hooper, “Norfloxacin: a new targeted fluoroquinolone antimicrobial agent,” Annals of Internal Medicine, vol. 108, no. 2, pp. 238–251, 1988. View at Publisher · View at Google Scholar
  40. B. F. Z. J. G. Feldman and V. C. Jain, Schalm’s Veterinary Hematology, Lippincott Williams and Wilkins, Philadilphia, 5th edition, 2000.
  41. S. A. Nassar, A. H. Mohamed, H. Soufy, and S. M. Nasr, “Protective effect of Egyptian propolis against rabbit pasteurellosis,” BioMed Research International, vol. 2013, Article ID 163724, 9 pages, 2013. View at Publisher · View at Google Scholar · View at Scopus
  42. Y. Watanabe, “Five cases of respiratory infection due to Pasteurella multocida,” Journal of the Japanese Association for Infectious Diseases, vol. 67, no. 12, pp. 1228–1232, 1993. View at Google Scholar
  43. R. P. Ruble, J. S. Cullor, and D. L. Brooks, “The observation of reactive thrombocytosis in New Zealand white rabbits in response to experimental Pasteurella multocida infection,” Blood Cells, Molecules, and Diseases, vol. 25, no. 2, pp. 95–102, 1999. View at Publisher · View at Google Scholar · View at Scopus
  44. P. E. Praveena, N. Singh, S. Periasamy, and A. Kumar, “Studies on haematobiochemical changes in Pasteurella multocida serotype A1 infection in mice,” Indian Journal of Veterinary Pathology, vol. 31, pp. 155–159, 2007. View at Google Scholar
  45. R. R. Cutler and P. Wilson, “Antibacterial activity of a new, stable, aqueous extract of allicin against methicillin-resistant Staphylococcus aureus,” British Journal of Biomedical Science, vol. 61, no. 2, pp. 71–74, 2004. View at Publisher · View at Google Scholar · View at Scopus
  46. D. C. Morrison, R. Silverstein, M. Luchi, and A. Shnyra, “Structure-function relationships of bacterial endotoxins: contribution to microbial sepsis,” Infectious Disease Clinics of North America, vol. 13, no. 2, pp. 313–340, 1999. View at Publisher · View at Google Scholar · View at Scopus
  47. O. Yoshie, T. Imai, and H. Nomiyama, “Chemokines in immunity,” Advances in Immunology, vol. 78, pp. 57–110, 2001. View at Publisher · View at Google Scholar · View at Scopus
  48. J. C. Hodgson, “Endotoxin and mammalian host responses during experimental disease,” Journal of Comparative Pathology, vol. 135, no. 4, pp. 157–175, 2006. View at Publisher · View at Google Scholar · View at Scopus
  49. W. M. El-Deeb and A. M. Elmoslemany, “The diagnostic accuracy of acute phase proteins and proinflammatory cytokines in sheep with pneumonic pasteurellosis,” PeerJ, vol. 4, article e2161, 2016. View at Publisher · View at Google Scholar · View at Scopus
  50. G. Kaplanski, V. Marin, F. Montero-Julian, A. Mantovani, and C. Farnarier, “IL-6: a regulator of the transition from neutrophil to monocyte recruitment during inflammation,” Trends in Immunology, vol. 24, no. 1, pp. 25–29, 2003. View at Publisher · View at Google Scholar · View at Scopus
  51. P. E. Praveena, S. Periasamy, A. A. Kumar, and N. Singh, “Cytokine profiles, apoptosis and pathology of experimental Pasteurella multocida serotype A1 infection in mice,” Research in Veterinary Science, vol. 89, no. 3, pp. 332–339, 2010. View at Publisher · View at Google Scholar · View at Scopus
  52. H. Salman, M. Bergman, H. Bessler, I. Punsky, and M. Djaldetti, “Effect of a garlic derivative (alliin) on peripheral blood cell immune responses,” International Journal of Immunopharmacology, vol. 21, no. 9, pp. 589–597, 1999. View at Publisher · View at Google Scholar · View at Scopus
  53. E. J. Nya and B. Austin, “Use of garlic, Allium sativum, to control Aeromonas hydrophila infection in rainbow trout, Oncorhynchus mykiss (Walbaum),” Journal of Fish Diseases, vol. 32, no. 11, pp. 963–970, 2009. View at Publisher · View at Google Scholar · View at Scopus
  54. E. J. Nya, Z. Dawood, and B. Austin, “The garlic component, allicin, prevents disease caused by Aeromonas hydrophila in rainbow trout, Oncorhynchus mykiss (Walbaum),” Journal of Fish Diseases, vol. 33, no. 4, pp. 293–300, 2010. View at Publisher · View at Google Scholar · View at Scopus
  55. Y. Feng, X. Zhu, Q. Wang et al., “Allicin enhances host pro-inflammatory immune responses and protects against acute murine malaria infection,” Malaria Journal, vol. 11, no. 1, p. 268, 2012. View at Publisher · View at Google Scholar · View at Scopus
  56. R. Bruck, H. Aeed, E. Brazovsky, T. Noor, and R. Hershkoviz, “Allicin, the active component of garlic, prevents immune-mediated, concanavalin A-induced hepatic injury in mice,” Liver International, vol. 25, no. 3, pp. 613–621, 2005. View at Publisher · View at Google Scholar · View at Scopus
  57. A. Makris, C. E. Thornton, B. Xu, and A. Hennessy, “Garlic increases IL-10 and inhibits TNFα and IL-6 production in endotoxin-stimulated human placental explants,” Placenta, vol. 26, no. 10, pp. 828–834, 2005. View at Publisher · View at Google Scholar · View at Scopus
  58. A. R. El-Sheakh, H. A. Ghoneim, G. M. Suddek, and E. S. M. Ammar, “Attenuation of oxidative stress, inflammation, and endothelial dysfunction in hypercholesterolemic rabbits by allicin,” Canadian Journal of Physiology and Pharmacology, vol. 94, no. 2, pp. 216–224, 2016. View at Publisher · View at Google Scholar
  59. E. Kyo, N. Uda, S. Kasuga, and Y. Itakura, “Immunomodulatory effects of aged garlic extract,” The Journal of Nutrition, vol. 131, no. 3, pp. 1075S–1079S, 2001. View at Publisher · View at Google Scholar
  60. R. O. A. Kamel and N. A. El-Shinnawy, “Immunomodulatory effect of garlic oil extract on Schistosoma mansoni infected mice,” Asian Pacific Journal of Tropical Medicine, vol. 8, no. 12, pp. 999–1005, 2015. View at Publisher · View at Google Scholar · View at Scopus
  61. Z. Jaglic, E. Jeklova, H. Christensen et al., “Host response in rabbits to infection with Pasteurella multocida serogroup F strains originating from fowl cholera,” Canadian Journal of Veterinary Research, vol. 75, no. 3, pp. 200–208, 2011. View at Google Scholar
  62. E. M. Leise, I. Gray, and M. K. Ward, “Leukocyte lactate dehydrogenase changes as an indicator of infection prior to overt symptoms,” Journal of Bacteriology, vol. 96, no. 1, pp. 154–159, 1968. View at Google Scholar
  63. E. M. Leise, F. LeSane, and I. Gray, “Lymphocyte and polymorphonuclear enzymes in stress: IV. Changes associated with an acute bacterial infection with Diplococcus pneumoniae,” Biochemical Medicine, vol. 9, no. 3, pp. 206–213, 1974. View at Publisher · View at Google Scholar · View at Scopus
  64. W. Abu El Hammed, H. Soufy, A. El-Shemy, S. M. Nasr, and M. I. Dessouky, “Use of allicin as feed additive to enhance vaccination capacity of Clostridium perfringens toxoid in rabbits,” Vaccine, vol. 34, no. 17, pp. 2000–2007, 2016. View at Publisher · View at Google Scholar · View at Scopus
  65. Y. Okada, K. Tanaka, E. Sato, and H. Okajima, “Kinetic and mechanistic studies of allicin as an antioxidant,” Organic & Biomolecular Chemistry, vol. 4, no. 22, pp. 4113–4117, 2006. View at Publisher · View at Google Scholar · View at Scopus
  66. L. Horev-Azaria, S. Eliav, N. Izigov et al., “Allicin up-regulates cellular glutathione level in vascular endothelial cells,” European Journal of Nutrition, vol. 48, no. 2, pp. 67–74, 2009. View at Publisher · View at Google Scholar · View at Scopus
  67. A. I. Abushouk, A. Ismail, A. M. A. Salem, A. M. Afifi, and M. M. Abdel-Daim, “Cardioprotective mechanisms of phytochemicals against doxorubicin-induced cardiotoxicity,” Biomedicine & Pharmacotherapy, vol. 90, pp. 935–946, 2017. View at Publisher · View at Google Scholar · View at Scopus
  68. J.-W. Zhu, T. Chen, J. Guan, W.-B. Liu, and J. Liu, “Neuroprotective effects of allicin on spinal cord ischemia–reperfusion injury via improvement of mitochondrial function in rabbits,” Neurochemistry International, vol. 61, no. 5, pp. 640–648, 2012. View at Publisher · View at Google Scholar · View at Scopus
  69. S. Shaban, M. W. A. El-Husseny, A. I. Abushouk, A. M. A. Salem, M. Mamdouh, and M. M. Abdel-Daim, “Effects of antioxidant supplements on the survival and differentiation of stem cells,” Oxidative Medicine and Cellular Longevity, vol. 2017, Article ID 5032102, 16 pages, 2017. View at Publisher · View at Google Scholar · View at Scopus