The Effects of Maternal Administration of Boswellia Gum Resin (Frankin-cense) during Lactation on Stereological Parameters of Rat Hippocampus

Document Type : Original Article (s)

Authors

1 Associate Professor, Department of Cell Biology and Anatomy, School of Medicine, Shahid Sadoughi University of Medical Sciences, Yazd, Iran

2 Professor, Department of Anatomical Sciences and Molecular Biology, School of Medicine, Isfahan University of Medical Sciences, Isfahan, Iran

Abstract

Background: We have previously reported that maternal administration of Boswellia serrata gum resin (Frankincense) during lactation increased learning and memory performance in young rat offsprings. This study aimed to determine the likely structural alterations of hippocampus, as a vital centre involved in learning and memory, following administration of Frankincense during lactationMethods: In this experimental study, 2 month-old male Wistar rats whose mothers were given oral aqueous extract of the Boswellia serrata (100 mg/kg/day) during lactation (3 weeks), and their controls whose mothers received saline (n = 6) were anesthetized and transcardially perfused. All brains were removed and divided into two hemispheres. One hemisphere was selected for estimating the volumes of cellular layers of hippocampus and the total number of neurons, and the other for estimating the individual somal volume. The Cavalieri's principle and an optical fractionator and a rotator were employed to estimate the volumes of layers, total number of neurons and individual neuronal volume, respectively.Findings: Our results showed that no significant difference in the total number of neurons in hippocampal subregions of the experimental group compared to the controls. However, the volume of cellular layer of dentate gyrus and cornu ammon 3(CA3) and individual volume of their neurons increased following maternal administration of Frankincense during lactation. Conclusion: The increased perikaryal volume in the hippocampal neurons of offsprings following maternal administration of Frankincense during lactation might be considered as an indicator of improved function of hippocampus, i.e. memory. It might be due to the increases in contents of neurons such as neurotransmitters, intracellular organelles or the number of synaptic contacts.

Keywords


  1. Archier P, Vieillescazes C. Characterisation of various geographical origin incense based on chemical criteria. Analusis 2000; 28(3): 233-7.
  2. Thulin M, Warfa AM. The frankincense trees (Boswellia spp., Burseraceae) of Northern Somalia and Southern Arabia. Kew Bulletin 1987; 42(3): 487-500.
  3. Ammon HP. Boswellic acids in chronic inflammatory diseases. Planta Med 2006; 72(12): 1100-16.
  4. Hamm S, Bleton J, Connan J, Tchapla A. A chemical investigation by headspace SPME and GC-MS of volatile and semi-volatile terpenes in various olibanum samples. Phytochemistry 2005; 66(12): 1499-514.
  5. Jauch J, Bergmann J. An efficient method for the large-scale preparation of 3-O-Acetyl-11-oxo-b-boswellic acid and other boswellic acids. Eur J Org Chem 2003; 2003(24): 4752-6.
  6. Moussaieff A, Shein NA, Tsenter J, Grigoriadis S, Simeonidou C, Alexandrovich AG, et al. Incensole acetate: a novel neuroprotective agent isolated from Boswellia carterii. J Cereb Blood Flow Metab 2008; 28(7): 1341-52.
  7. Moussaieff A, Rimmerman N, Bregman T, Straiker A, Felder CC, Shoham S, et al. Incensole acetate, an incense component, elicits psychoactivity by activating TRPV3 channels in the brain. FASEB J 2008; 22(8): 3024-34.
  8. Altmann A, Poeckel D, Fischer L, Schubert-Zsilavecz M, Steinhilber D, Werz O. Coupling of boswellic acid-induced Ca2+ mobilisation and MAPK activation to lipid metabolism and peroxide formation in human leucocytes. Br J Pharmacol 2004; 141(2): 223-32.
  9. Poeckel D, Tausch L, Altmann A, Feisst C, Klinkhardt U, Graff J, et al. Induction of central signalling pathways and select functional effects in human platelets by beta-boswellic acid. Br J Pharmacol 2005; 146(4): 514-24.
  10. Moore PD. Conservation biology: unkind cuts for incense. Nature 2006; 444(7121): 829.
  11. Ernst E. Frankincense: systematic review. BMJ 2008; 337: a2813.
  12. Moussaieff A, Shohami E, Kashman Y, Fride E, Schmitz ML, Renner F, et al. Incensole acetate, a novel anti-inflammatory compound isolated from Boswellia resin, inhibits nuclear factor-kappa B activation. Mol Pharmacol 2007; 72(6): 1657-64.
  13. Menon MK, Kar A. Analgesic and psychopharmacological effects of the gum resin of Boswellia serrata. Planta Med 1971; 19(4): 333-41.
  14. Dixit VP, Joshi S, Sinha R, Bharvava SK, Varma M. Hypolipidemic activity of guggal resin (Commiphora mukul) and garlic (Alium sativum linn.) in dogs (Canis familiaris) and monkeys (Presbytis entellus entellus Dufresne). Biochem Exp Biol 1980; 16(4): 421-4.
  15. Huang MT, Badmaev V, Ding Y, Liu Y, Xie JG, Ho CT. Anti-tumor and anti-carcinogenic activities of triterpenoid, beta-boswellic acid. Biofactors 2000; 13(1-4): 225-30.
  16. Abdul Hameed H. Avicenna's Tract on Cardiac Drugs and Essays on Arab Cardiotherapy. New Delhi: Hamdard Foundation; 1983.
  17. Marshall S. Frankincense: festive pharmacognosy. Pharm J 2003; 271: 862-4.
  18. Mahmoudi A, Hosseini-Sharifabad A, Monsef-Esfahani HR, Yazdinejad AR, Khanavi M, Roghani A, et al. Evaluation of systemic administration of Boswellia papyrifera extracts on spatial memory retention in male rats. J Nat Med 2011; 65(3-4): 519-25.
  19. Farshchi A, Ghiasi G, Farshchi S, Malek Khatabi P. Effects of boswellia papyrifera gum extract on learning and memory in mice and rats. Iran J Basic Med Sci 2010; 13(2): 9-15.
  20. Hosseini M, Hadjzadeh MA, Derakhshan M, Havakhah S, Rassouli FB, Rakhshandeh H, et al. The beneficial effects of olibanum on memory deficit induced by hypothyroidism in adult rats tested in Morris water maze. Arch Pharm Res 2010; 33(3): 463-8.
  21. Buchele B, Zugmaier W, Estrada A, Genze F, Syrovets T, Paetz C, et al. Characterization of 3alpha-acetyl-11-keto-alpha-boswellic acid, a pentacyclic triterpenoid inducing apoptosis in vitro and in vivo. Planta Med 2006; 72(14): 1285-9.
  22. Hosseini-Sharifabad M, Esfandiari E, Alaei H. Effects of Frankincence aqueous extract during gestational period on increasing power of learning and memory in adult offsprings. Journal of Isfahan Medical School 2004; 21(71): 16-20.
  23. Hosseini-Sharifabad M, Esfandiary E. Effect of maternal consumption of aqueous extract of the gum resin of Boswellia Serrata during lactation on increasing power of learning and memory in adult offsprings. Iran J Basic Med Sc 2003; 6(3): 207-11.
  24. Hosseini-Sharifabad M, Esfandiary E. Quantitative analysis of hippocampal neuron number and size following prenatal administration of Boswellia serrata gum resin in adult rats. Journal of Isfahan Medical School 2005; 21(76-77): 58-63.
  25. Hosseini-Sharifabad M, Esfandiary E. A morphometeric study on CA3 hippocampal field in young rats following maternal administration of Boswellia serrata resin during gestation. Iran J Basic Med Sci 2007; 10(3): 176-82.
  26. Bayer SA, Altman J, Russo RJ, Zhang X. Timetables of neurogenesis in the human brain based on experimentally determined patterns in the rat. Neurotoxicology 1993; 14(1): 83-144.
  27. Zola-Morgan S, Squire LR. Neuroanatomy of memory. Annu Rev Neurosci 1993; 16: 547-63.
  28. West MJ, Slomianka L, Gundersen HJ. Unbiased stereological estimation of the total number of neurons in thesubdivisions of the rat hippocampus using the optical fractionator. Anat Rec 1991; 231(4): 482-97.
  29. Gundersen HJ, Bendtsen TF, Korbo L, Marcussen N, Moller A, Nielsen K, et al. Some new, simple and efficient stereological methods and their use in pathological research and diagnosis. APMIS 1988; 96(5): 379-94.
  30. Ammon HP, Mack T, Singh GB, Safayhi H. Inhibition of leukotriene B4 formation in rat peritoneal neutrophils by an ethanolic extract of the gum resin exudate of Boswellia serrata. Planta Med 1991; 57(3): 203-7.
  31. Hosseini-Sharifabad M, Nyengaard JR. Design-based estimation of neuronal number and individual neuronal volume in the rat hippocampus. J Neurosci Methods 2007; 162(1-2): 206-14.
  32. Tandrup T, Gundersen HJ, Jensen EB. The optical rotator. J Microsc 1997; 186(Pt 2): 108-20.
  33. Gundersen HJ, Jensen EB, Kieu K, Nielsen J. The efficiency of systematic sampling in stereology--reconsidered. J Microsc 1999; 193(Pt 3): 199-211.
  34. West MJ, Gundersen HJ. Unbiased stereological estimation of the number of neurons in the human hippocampus. J Comp Neurol 1990; 296(1): 1-22.
  35. Arnold SE, Franz BR, Gur RC, Gur RE, Shapiro RM, Moberg PJ, et al. Smaller neuron size in schizophrenia in hippocampal subfields that mediate cortical-hippocampal interactions. Am J Psychiatry 1995; 152(5): 738-48.
  36. Insausti AM, Gaztelu JM, Gonzalo LM, Romero-Vives M, Barrenechea C, Felipo V, et al. Diet induced hyperammonemia decreases neuronal nuclear size in rat entorhinal cortex. Neurosci Lett 1997; 231(3): 179-81.
  37. Poeckel D, Werz O. Boswellic acids: biological actions and molecular targets. Curr Med Chem 2006; 13(28): 3359-69.
  38. Nguyen PV, Woo NH. Regulation of hippocampal synaptic plasticity by cyclic AMP-dependent protein kinases. Prog Neurobiol 2003; 71(6): 401-37.
  39. Alkon DL, Sun MK, Nelson TJ. PKC signaling deficits: a mechanistic hypothesis for the origins of Alzheimer's disease. Trends Pharmacol Sci 2007; 28(2): 51-60.
  40. Sharifzadeh M, Aghsami M, Gholizadeh S, Tabrizian K, Soodi M, Khalaj S, et al. Protective effects of chronic lithium treatment against spatial memory retention deficits induced by the protein kinase AII inhibitor H-89 in rats. Pharmacology 2007; 80(2-3): 158-65.
  41. Sharifzadeh M, Sharifzadeh K, Naghdi N, Ghahremani MH, Roghani A. Posttraining intrahippocampal infusion of a protein kinase AII inhibitor impairs spatial memory retention in rats. J Neurosci Res 2005; 79(3): 392-400.
  42. Van HT, Cole G, Katzman R, Huang KP, Saitoh T. Reduced protein kinase C immunoreactivity and altered protein phosphorylation in Alzheimer's disease fibroblasts. Arch Neurol 1989; 46(11): 1195-9.
  43. Karima O, Riazi G, Yousefi R, Movahedi AA. The enhancement effect of beta-boswellic acid on hippocampal neurites outgrowth and branching (an in vitro study). Neurol Sci 2010; 31(3): 315-20.