Effects of Tualang honey in modulating nociceptive responses at the spinal cord in offspring of prenatally stressed rats
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摘要
Objective: This study was done to determine whether Tualang honey could prevent the altered nociceptive behaviour, with its associated changes of oxidative stress markers and morphology of the spinal cord,among the offspring of prenatally stressed rats.Methods: Pregnant rats were divided into three groups: control, stress, and stress treated with Tualang honey. The stress and stress treated with Tualang honey groups were subjected to restraint stress from day 11 of pregnancy until delivery. Ten week old male offspring(n = 9 from each group) were given formalin injection and their nociceptive behaviours were recorded. After 2 h, the rats were sacrificed, and their spinal cords were removed to assess oxidative stress activity and morphology. Nociceptive behaviour was analysed using repeated measures analysis of variance(ANOVA), while the levels of oxidative stress parameters and number of Nissl-stained neurons were analysed using a one-way ANOVA.Results: This study demonstrated that prenatal stress was associated with increased nociceptive behaviour, changes in the oxidative stress parameters and morphology of the spinal cord of offspring exposed to prenatal stress; administration of Tualang honey reduced the alteration of these parameters.Conclusion: This study provides a preliminary understanding of the beneficial effects of Tualang honey against the changes in oxidative stress and neuronal damage in the spinal cord of the offspring of prenatally stressed rats.
Objective: This study was done to determine whether Tualang honey could prevent the altered nociceptive behaviour, with its associated changes of oxidative stress markers and morphology of the spinal cord,among the offspring of prenatally stressed rats.Methods: Pregnant rats were divided into three groups: control, stress, and stress treated with Tualang honey. The stress and stress treated with Tualang honey groups were subjected to restraint stress from day 11 of pregnancy until delivery. Ten week old male offspring(n = 9 from each group) were given formalin injection and their nociceptive behaviours were recorded. After 2 h, the rats were sacrificed, and their spinal cords were removed to assess oxidative stress activity and morphology. Nociceptive behaviour was analysed using repeated measures analysis of variance(ANOVA), while the levels of oxidative stress parameters and number of Nissl-stained neurons were analysed using a one-way ANOVA.Results: This study demonstrated that prenatal stress was associated with increased nociceptive behaviour, changes in the oxidative stress parameters and morphology of the spinal cord of offspring exposed to prenatal stress; administration of Tualang honey reduced the alteration of these parameters.Conclusion: This study provides a preliminary understanding of the beneficial effects of Tualang honey against the changes in oxidative stress and neuronal damage in the spinal cord of the offspring of prenatally stressed rats.
Objective: This study was done to determine whether Tualang honey could prevent the altered nociceptive behaviour, with its associated changes of oxidative stress markers and morphology of the spinal cord,among the offspring of prenatally stressed rats.Methods: Pregnant rats were divided into three groups: control, stress, and stress treated with Tualang honey. The stress and stress treated with Tualang honey groups were subjected to restraint stress from day 11 of pregnancy until delivery. Ten week old male offspring(n = 9 from each group) were given formalin injection and their nociceptive behaviours were recorded. After 2 h, the rats were sacrificed, and their spinal cords were removed to assess oxidative stress activity and morphology. Nociceptive behaviour was analysed using repeated measures analysis of variance(ANOVA), while the levels of oxidative stress parameters and number of Nissl-stained neurons were analysed using a one-way ANOVA.Results: This study demonstrated that prenatal stress was associated with increased nociceptive behaviour, changes in the oxidative stress parameters and morphology of the spinal cord of offspring exposed to prenatal stress; administration of Tualang honey reduced the alteration of these parameters.Conclusion: This study provides a preliminary understanding of the beneficial effects of Tualang honey against the changes in oxidative stress and neuronal damage in the spinal cord of the offspring of prenatally stressed rats.
引文
[1]Van den Bergh BR,Mulder EJ,Mennes M,Glover V.Antenatal maternal anxiety and stress and the neurobehavioural development of the fetus and child:links and possible mechanisms.A review.Neurosci Biobehav Rev 2005;29(2):237-58.
[2]Charil A,Laplante DP,Vaillancourt C,King S.Prenatal stress and brain development.Brain Res Rev 2010;65(1):56-79.
[3]Hultman CM,Ohman A,Cnattingius S,Wieselgren IM,Lindstrom LH.Prenatal and neonatal risk factors for schizophrenia.Br J Psychiatry 1997;170:128-33.
[4]Ward AJ.Prenatal stress and childhood psychopathology.Child Psychiatry Hum Dev 1991;22(2):97-110.
[5]Abd Aziz CB,Ahmad R,Mohamed M,Wan Yusof WN.The effects of Tualang honey intake during prenatal stress on pain responses in the rat offspring.Eur JIntegr Med 2013;5:326-31.
[6]Sternberg WF,Ridgway CG.Effects of gestational stress and neonatal handling on pain,analgesia,and stress behavior of adult mice.Physiol Behav 2003;78(3):375-83.
[7]Butkevich IP,Barr GA,Mikhailenko VA,Otellin VA.Increased formalin-induced pain and expression of Fos neurons in the lumbar spinal cord of prenatally stressed infant rats.Neurosci Lett 2006;403(3):222-6.
[8]Austin MP,Hadzi-Pavlovic D,Leader L,Saint K,Parker G.Maternal trait anxiety,depression and life event stress in pregnancy:relationships with infant temperament.Earl Hum Dev 2005;81(2):183-90.
[9]Mulder EJ,Robles De Medina PG,Huizink AC,Van den Bergh BR,Buitelaar JK,Visser GH.Prenatal maternal stress:effects on pregnancy and the(unborn)child.Earl Hum Dev 2002;70(1-2):3-14.
[10]Mairesse J,Lesage J,Breton C,Bréant B,Hahn T,Darnaudéry M,et al.Maternal stress alters endocrine function of the feto-placental unit in rats.Am J Physiol Endocrinol Metab 2007;292(6):E1526-33.
[11]Sahu S,Madhyastha S,Rao G.Effect of prenatal stress on expression of glutathione system in neonatal rat brain.Turk Neurosurg 2012;22(5):576-82.
[12]Zafi A,Banu N.Modulation of in vivo oxidative status by exogenous corticosterone and restraint stress in rats.Stress 2009;12(2):167-77.
[13]Bingham BC,Sheela Rani CS,Frazer A,Strong R,Morilak DA.Exogenous prenatal corticosterone exposure mimics the effects of prenatal stress on adult brain stress response systems and fear extinction behavior.Psychoneuroendocrinology 2013;38(11):2746-57.
[14]Kishore RK,Halim AS,Syazana MN,Sirajudeen K.Tualang honey has higher phenolic content and greater radical scavenging activity compared with other honey sources.Nut Res 2011;31(4):322-5.
[15]Al-Rahbi B,Zakaria R,Othman Z,Hassan A,Ahmad AH.Protective effects of Tualang honey against oxidative stress and anxiety-like behaviour in stressed ovariectomized rats.Int Sch Res Notices 2014:521065.
[16]Erejuwa OO,Sulaiman SA,Wahab MS,Sirajudeen KN,Salleh MS,Gurtu S.Antioxidant protection of Malaysian Tualang honey in pancreas of normal and streptozotocin-induced diabetic rats.Ann Endocrinol(Paris)2010;71(4):291-6.
[17]Aziz CB,Ismail CAN,Hussin CM,Mohamed M.The antinociceptive effects of Tualang honey in male Sprague-Dawley rats:a preliminary study.J Trad Comp Med 2014;4(4):298-302.
[18]Butkevich I,Mikhailenko V,Semionov P,Bagaeva T,Otellin V,Aloisi AM.Effects of maternal corticosterone and stress on behavioral and hormonal indices of formalin pain in male and female offspring of different ages.Horm Behav2009;55(1):149-57.
[19]Hayati AA,Zalina I,Myo T,Badariah AA,Azhar A,Idris L.Modulation of formalin-induced fos-like immunoreactivity in the spinal cord by swim stressinduced analgesia,morphine and ketamine.Ger Med Sci 2008;6:Doc05.
[20]Dubuisson D,Dennis SG.The formalin test:a quantitative study of the analgesic effects of morphine,meperidine,and brain stem stimulation in rats and cats.Pain 1977;4(2):161-74.
[21]Gim GT,Lee JH,Park E,Sung YH,Kim CJ,Hwang WW,et al.Electroacupuncture attenuates mechanical and warm allodynia through suppression of spinal glial activation in a rat model of neuropathic pain.Brain Res Bull 2011;86(5-6):403-11.
[22]Shibata M,Ohkubo T,Takashi H,Inoki R.Modified formalin test:characteristic biphasic pain response.Pain 1989;38(3):347-52.
[23]Tj?lsen A,Berge OG,Hunskaar S,Rosland JH,Hole K.The formalin test:an evaluation of the method.Pain 1992;51(1):5-17.
[24]Stohr T,Schulte Wermeling D,Szuran T,Pliska V,Domeney A,Welzl H,et al.Differential effects of prenatal stress in two inbred strains of rats.Pharmacol Biochem Behav 1998;59(4):799-805.
[25]Butkevich IP,Barr GA,Mikhailenko VA.Effect of prenatal stress on serotonergic neurons in dorsal raphe nucleus and on pain behavior during neonatal period.Ross Fiziol Zh Im I M Sechenova 2015;101(7):758-68[Russian].
[26]Wang CY,Hung CH,Lin CS,Lee HH,Yang CH,Jong YJ,et al.Differential alterations of GABAAreceptor(a1,b2,c2 subunit)expression and increased seizure susceptibility in rat offspring from morphine-addicted mothers:beneficial effect of dextromethorphan.Neurosci Lett 2011;489(1):5-9.
[27]Tavassoli E,Saboory E,Teshfam M,Rasmi Y,Roshan-Milani S,Ilkhanizadeh B,et al.Effect of prenatal stress on density of NMDA receptors in rat brain.Int JDev Neurosci 2013;31(8):790-5.
[28]Wei H,Hao B,Huang JL,Ma AN,Li XY,Wang YX,et al.Intrathecal administration of a gap junction decoupler,an inhibitor of Na+-K+-2Clcotransporter 1,or a GABAAreceptor agonist attenuates mechanical pain hypersensitivity induced by REM sleep deprivation in the rat.Pharmacol Biochem Behav 2010;97(2):377-83.
[29]Reyes RC,Brennan AM,Shen Y,Baldwin Y,Swanson RA.Activation of neuronal NMDA receptors induces superoxide-mediated oxidative stress in neighboring neurons and astrocytes.J Neurosci 2012;32(37):12973-8.
[30]Brittain MK,Brustovetsky T,Sheets PL,Brittain JM,Khanna R,Cummins TR,et al.Delayed calcium dysregulation in neurons requires both the NMDAreceptor and the reverse Na+/Ca2+exchanger.Neurobiol Dis 2012;46(1):109-17.
[31]Betzen C,White R,Zehendne CM,Pietrowski E,Bender B,Luhmann HJ,et al.Oxidative stress upregulates the NMDA receptor on cerebrovascular endothelium.Free Radic Biol Med 2009;47(8):1212-20.
[32]Narenjkar J,Roghani M,Alambeygi H,Sedaghati F.The effect of the flavonoid quercetin on pain sensation in diabetic rats.Basic Clin Neurosci 2011;2(3):51-7.
[33]Azevedo MI,Pereira AF,Nogueira RB,Rolim FE,Brito GA,Wong DV.The antioxidant effects of the flavonoids rutin and quercetin inhibit oxaliplatininduced chronic painful peripheral neuropathy.Mol Pain 2013;9:53.
[34]Schroder-van der Elst JP,van der Heide D,Rokos H,Morreale de Escobar G,Kohrle J.Synthetic flavonoids cross the placenta in the rat and are found in fetal brain.Am J Physiol 1998;274(2 Pt.1):E253-6.
[35]Madhyastha S,Sahu SS,Rao G.Resveratrol for prenatal-stress-induced oxidative damage in growing brain and its consequences on survival of neurons.J Basic Clin Physiol Pharmacol 2014;25(1):63-72.
[36]Zhu Z,Li X,Chen W,Zhao Y,Li H,Qing C,et al.Prenatal stress causes genderdependent neuronal loss and oxidative stress in rat hippocampus.J Neurosci Res 2004;78(6):837-44.
[37]Duthie L,Reynold RM.Changes in the maternal hypothalamic-pituitaryadrenal axis in pregnancy and postpartum:influences on maternal and fetal outcomes.Neuroendocrinology 2013;98(2):106-15.
[38]Slotkin TA,Barnes GA,McCook EC,Seidler FJ.Programming of brainstem serotonin transporter development by prenatal glucocorticoids.Brain Res Dev Brain Res 1996;93(1-2):155-61.
[39]Diaz R,Ogren SO,Blum M,Fuxe K.Prenatal corticosterone increases spontaneous and d-amphetamine induced locomotor activity and brain dopamine metabolism in prepubertal male and female rats.Neuroscience1995;66(2):467-73.
[40]Sheline YI,Wang PW,Gado MH,Csernansky JG,Vannier MW.Hippocampal atrophy in recurrent major depression.Proc Natl Acad Sci U S A 1996;93(9):3908-13.
[41]You JM,Yun SJ,Nam KN,Kang C,Won R,Lee EH.Mechanism of glucocorticoidinduced oxidative stress in rat hippocampal slice cultures.Can J Physiol Pharmacol 2009;87(6):440-7.
[42]Bose R,Moors M,Tofighi R,Cascante A,Hermanson O,Ceccatelli S.Glucocorticoids induce long-lasting effects in neural stem cells resulting in senescence-related alterations.Cell Death Dis 2010;1:e92.
[43]Fu KY,Light AR,Maixner W.Long-lasting inflammation and long-term hyperalgesia after subcutaneous formalin injection into the rat hindpaw.JPain 2001;2(1):2-11.
[44]Gohil JT,Patel PK,Gupta P.Evaluation of oxidative stress and antioxidant defence in subjects of preeclampsia.J Obstet Gynaecol India 2011;61(6):638-40.
[45]Vega CC,Reyes-Castro LA,Rodríguez-González GL,Bautista CJ,VázquezMartínez M,Larrea F,et al.Resveratrol partially prevents oxidative stress and metabolic dysfunction in pregnant rats fed a low protein diet and their offspring.J Physiol 2016;594(5):1483-99.
[46]Al-Amin MM,Alam T,Hasan SM,Hasan AT,Quddus AH.Prenatal maternal lipopolysaccharide administration leads to age-and region-specific oxidative stress in the early developmental stage in offspring.Neuroscience 2016;318:84-93.
[47]Dringen R,Hirrlinger J.Glutathione pathways in the brain.Biol Chem2003;384(4):505-16.
[48]Bounous G,Molson JH.The antioxidant system.Anticancer Res 2003;23(2B):1411-5.
[49]Khalil MI,Alam N,Moniruzzaman M,Sulaiman SA,Gan SH.Phenolic acid composition and antioxidant properties of Malaysian honeys.J Food Sci2011;76(6):C921-8.
[50]Kawabata K,Kawai Y,Terao J.Suppressive effect of quercetin on acute stressinduced hypothalamic-pituitary-adrenal axis response in Wistar rats.J Nutr Biochem 2010;21(5):374-80.
[2]Charil A,Laplante DP,Vaillancourt C,King S.Prenatal stress and brain development.Brain Res Rev 2010;65(1):56-79.
[3]Hultman CM,Ohman A,Cnattingius S,Wieselgren IM,Lindstrom LH.Prenatal and neonatal risk factors for schizophrenia.Br J Psychiatry 1997;170:128-33.
[4]Ward AJ.Prenatal stress and childhood psychopathology.Child Psychiatry Hum Dev 1991;22(2):97-110.
[5]Abd Aziz CB,Ahmad R,Mohamed M,Wan Yusof WN.The effects of Tualang honey intake during prenatal stress on pain responses in the rat offspring.Eur JIntegr Med 2013;5:326-31.
[6]Sternberg WF,Ridgway CG.Effects of gestational stress and neonatal handling on pain,analgesia,and stress behavior of adult mice.Physiol Behav 2003;78(3):375-83.
[7]Butkevich IP,Barr GA,Mikhailenko VA,Otellin VA.Increased formalin-induced pain and expression of Fos neurons in the lumbar spinal cord of prenatally stressed infant rats.Neurosci Lett 2006;403(3):222-6.
[8]Austin MP,Hadzi-Pavlovic D,Leader L,Saint K,Parker G.Maternal trait anxiety,depression and life event stress in pregnancy:relationships with infant temperament.Earl Hum Dev 2005;81(2):183-90.
[9]Mulder EJ,Robles De Medina PG,Huizink AC,Van den Bergh BR,Buitelaar JK,Visser GH.Prenatal maternal stress:effects on pregnancy and the(unborn)child.Earl Hum Dev 2002;70(1-2):3-14.
[10]Mairesse J,Lesage J,Breton C,Bréant B,Hahn T,Darnaudéry M,et al.Maternal stress alters endocrine function of the feto-placental unit in rats.Am J Physiol Endocrinol Metab 2007;292(6):E1526-33.
[11]Sahu S,Madhyastha S,Rao G.Effect of prenatal stress on expression of glutathione system in neonatal rat brain.Turk Neurosurg 2012;22(5):576-82.
[12]Zafi A,Banu N.Modulation of in vivo oxidative status by exogenous corticosterone and restraint stress in rats.Stress 2009;12(2):167-77.
[13]Bingham BC,Sheela Rani CS,Frazer A,Strong R,Morilak DA.Exogenous prenatal corticosterone exposure mimics the effects of prenatal stress on adult brain stress response systems and fear extinction behavior.Psychoneuroendocrinology 2013;38(11):2746-57.
[14]Kishore RK,Halim AS,Syazana MN,Sirajudeen K.Tualang honey has higher phenolic content and greater radical scavenging activity compared with other honey sources.Nut Res 2011;31(4):322-5.
[15]Al-Rahbi B,Zakaria R,Othman Z,Hassan A,Ahmad AH.Protective effects of Tualang honey against oxidative stress and anxiety-like behaviour in stressed ovariectomized rats.Int Sch Res Notices 2014:521065.
[16]Erejuwa OO,Sulaiman SA,Wahab MS,Sirajudeen KN,Salleh MS,Gurtu S.Antioxidant protection of Malaysian Tualang honey in pancreas of normal and streptozotocin-induced diabetic rats.Ann Endocrinol(Paris)2010;71(4):291-6.
[17]Aziz CB,Ismail CAN,Hussin CM,Mohamed M.The antinociceptive effects of Tualang honey in male Sprague-Dawley rats:a preliminary study.J Trad Comp Med 2014;4(4):298-302.
[18]Butkevich I,Mikhailenko V,Semionov P,Bagaeva T,Otellin V,Aloisi AM.Effects of maternal corticosterone and stress on behavioral and hormonal indices of formalin pain in male and female offspring of different ages.Horm Behav2009;55(1):149-57.
[19]Hayati AA,Zalina I,Myo T,Badariah AA,Azhar A,Idris L.Modulation of formalin-induced fos-like immunoreactivity in the spinal cord by swim stressinduced analgesia,morphine and ketamine.Ger Med Sci 2008;6:Doc05.
[20]Dubuisson D,Dennis SG.The formalin test:a quantitative study of the analgesic effects of morphine,meperidine,and brain stem stimulation in rats and cats.Pain 1977;4(2):161-74.
[21]Gim GT,Lee JH,Park E,Sung YH,Kim CJ,Hwang WW,et al.Electroacupuncture attenuates mechanical and warm allodynia through suppression of spinal glial activation in a rat model of neuropathic pain.Brain Res Bull 2011;86(5-6):403-11.
[22]Shibata M,Ohkubo T,Takashi H,Inoki R.Modified formalin test:characteristic biphasic pain response.Pain 1989;38(3):347-52.
[23]Tj?lsen A,Berge OG,Hunskaar S,Rosland JH,Hole K.The formalin test:an evaluation of the method.Pain 1992;51(1):5-17.
[24]Stohr T,Schulte Wermeling D,Szuran T,Pliska V,Domeney A,Welzl H,et al.Differential effects of prenatal stress in two inbred strains of rats.Pharmacol Biochem Behav 1998;59(4):799-805.
[25]Butkevich IP,Barr GA,Mikhailenko VA.Effect of prenatal stress on serotonergic neurons in dorsal raphe nucleus and on pain behavior during neonatal period.Ross Fiziol Zh Im I M Sechenova 2015;101(7):758-68[Russian].
[26]Wang CY,Hung CH,Lin CS,Lee HH,Yang CH,Jong YJ,et al.Differential alterations of GABAAreceptor(a1,b2,c2 subunit)expression and increased seizure susceptibility in rat offspring from morphine-addicted mothers:beneficial effect of dextromethorphan.Neurosci Lett 2011;489(1):5-9.
[27]Tavassoli E,Saboory E,Teshfam M,Rasmi Y,Roshan-Milani S,Ilkhanizadeh B,et al.Effect of prenatal stress on density of NMDA receptors in rat brain.Int JDev Neurosci 2013;31(8):790-5.
[28]Wei H,Hao B,Huang JL,Ma AN,Li XY,Wang YX,et al.Intrathecal administration of a gap junction decoupler,an inhibitor of Na+-K+-2Clcotransporter 1,or a GABAAreceptor agonist attenuates mechanical pain hypersensitivity induced by REM sleep deprivation in the rat.Pharmacol Biochem Behav 2010;97(2):377-83.
[29]Reyes RC,Brennan AM,Shen Y,Baldwin Y,Swanson RA.Activation of neuronal NMDA receptors induces superoxide-mediated oxidative stress in neighboring neurons and astrocytes.J Neurosci 2012;32(37):12973-8.
[30]Brittain MK,Brustovetsky T,Sheets PL,Brittain JM,Khanna R,Cummins TR,et al.Delayed calcium dysregulation in neurons requires both the NMDAreceptor and the reverse Na+/Ca2+exchanger.Neurobiol Dis 2012;46(1):109-17.
[31]Betzen C,White R,Zehendne CM,Pietrowski E,Bender B,Luhmann HJ,et al.Oxidative stress upregulates the NMDA receptor on cerebrovascular endothelium.Free Radic Biol Med 2009;47(8):1212-20.
[32]Narenjkar J,Roghani M,Alambeygi H,Sedaghati F.The effect of the flavonoid quercetin on pain sensation in diabetic rats.Basic Clin Neurosci 2011;2(3):51-7.
[33]Azevedo MI,Pereira AF,Nogueira RB,Rolim FE,Brito GA,Wong DV.The antioxidant effects of the flavonoids rutin and quercetin inhibit oxaliplatininduced chronic painful peripheral neuropathy.Mol Pain 2013;9:53.
[34]Schroder-van der Elst JP,van der Heide D,Rokos H,Morreale de Escobar G,Kohrle J.Synthetic flavonoids cross the placenta in the rat and are found in fetal brain.Am J Physiol 1998;274(2 Pt.1):E253-6.
[35]Madhyastha S,Sahu SS,Rao G.Resveratrol for prenatal-stress-induced oxidative damage in growing brain and its consequences on survival of neurons.J Basic Clin Physiol Pharmacol 2014;25(1):63-72.
[36]Zhu Z,Li X,Chen W,Zhao Y,Li H,Qing C,et al.Prenatal stress causes genderdependent neuronal loss and oxidative stress in rat hippocampus.J Neurosci Res 2004;78(6):837-44.
[37]Duthie L,Reynold RM.Changes in the maternal hypothalamic-pituitaryadrenal axis in pregnancy and postpartum:influences on maternal and fetal outcomes.Neuroendocrinology 2013;98(2):106-15.
[38]Slotkin TA,Barnes GA,McCook EC,Seidler FJ.Programming of brainstem serotonin transporter development by prenatal glucocorticoids.Brain Res Dev Brain Res 1996;93(1-2):155-61.
[39]Diaz R,Ogren SO,Blum M,Fuxe K.Prenatal corticosterone increases spontaneous and d-amphetamine induced locomotor activity and brain dopamine metabolism in prepubertal male and female rats.Neuroscience1995;66(2):467-73.
[40]Sheline YI,Wang PW,Gado MH,Csernansky JG,Vannier MW.Hippocampal atrophy in recurrent major depression.Proc Natl Acad Sci U S A 1996;93(9):3908-13.
[41]You JM,Yun SJ,Nam KN,Kang C,Won R,Lee EH.Mechanism of glucocorticoidinduced oxidative stress in rat hippocampal slice cultures.Can J Physiol Pharmacol 2009;87(6):440-7.
[42]Bose R,Moors M,Tofighi R,Cascante A,Hermanson O,Ceccatelli S.Glucocorticoids induce long-lasting effects in neural stem cells resulting in senescence-related alterations.Cell Death Dis 2010;1:e92.
[43]Fu KY,Light AR,Maixner W.Long-lasting inflammation and long-term hyperalgesia after subcutaneous formalin injection into the rat hindpaw.JPain 2001;2(1):2-11.
[44]Gohil JT,Patel PK,Gupta P.Evaluation of oxidative stress and antioxidant defence in subjects of preeclampsia.J Obstet Gynaecol India 2011;61(6):638-40.
[45]Vega CC,Reyes-Castro LA,Rodríguez-González GL,Bautista CJ,VázquezMartínez M,Larrea F,et al.Resveratrol partially prevents oxidative stress and metabolic dysfunction in pregnant rats fed a low protein diet and their offspring.J Physiol 2016;594(5):1483-99.
[46]Al-Amin MM,Alam T,Hasan SM,Hasan AT,Quddus AH.Prenatal maternal lipopolysaccharide administration leads to age-and region-specific oxidative stress in the early developmental stage in offspring.Neuroscience 2016;318:84-93.
[47]Dringen R,Hirrlinger J.Glutathione pathways in the brain.Biol Chem2003;384(4):505-16.
[48]Bounous G,Molson JH.The antioxidant system.Anticancer Res 2003;23(2B):1411-5.
[49]Khalil MI,Alam N,Moniruzzaman M,Sulaiman SA,Gan SH.Phenolic acid composition and antioxidant properties of Malaysian honeys.J Food Sci2011;76(6):C921-8.
[50]Kawabata K,Kawai Y,Terao J.Suppressive effect of quercetin on acute stressinduced hypothalamic-pituitary-adrenal axis response in Wistar rats.J Nutr Biochem 2010;21(5):374-80.