@2024 Afarand., IRAN
ISSN: 2252-0805 The Horizon of Medical Sciences 2014;20(1):53-57
ISSN: 2252-0805 The Horizon of Medical Sciences 2014;20(1):53-57
Effect of prenatal stresses on the response to pain in rats
ARTICLE INFO
Article Type
Original ResearchAuthors
Soufi Abadi M. (1)HaghdoostYazdi H. (*)
Abbasnezhad A.A. (2)
Amoli N. (3)
Ghadimi F. (3)
(*) Physiology Department, Medicine Faculty, Qazvin University of Medical Sciences, Qazvin, Iran
(1) Physiology Department, Medicine Faculty, Qazvin University of Medical Sciences, Qazvin, Iran
(2) Basic Sciences Department, Medicine Faculty, Gonabad University of Medical Sciences, Gonabad, Iran
(3) Anestetist Department, Paramedical Faculty, Qazvin University of Medical Sciences, Qazvin, Iran
Correspondence
Address: Physiology Department, Medicine Faculty, Qazvin University of Medical Sciences, Shahid Bahonar Boulevard, Qazvin, IranPhone: +982813336001
Fax: +982813324971
hhaghdoost@yahoo.com
Article History
Received: October 20, 2013Accepted: March 6, 2014
ePublished: April 1, 2014
BRIEF TEXT
During pregnancy, stress is a potential cause of neurological diseases for the mother and fetus [1]. It may result in shift in hypothalamic-pituitary-adrenal axis activity during fetal period and after that [2]. Having impact on brain’s structure and function, this disorder disturbs after birth processes of nervous system.
According to some studies, gender and time-dependent fetal stress among rats intensifies induced seizures by pilocarpine, and raises corticosterone level in blood [3]. In addition, stress during pregnancy may results in changes in brain evolution, and disturbs stable performance of brain via creating unusual neuronal communication [4]. Results of a conducted study show that during pregnancy, some stressors affect brain evolution, head circumference, and fetal weight at birth [5]. According to conducted researches, facing with types of physical-environmental stresses in fetal period affects behavioral responds to different environmental stimuli. Intensity of pain sensation may change by stress [8]. However, impact of stress in fetal period on pain threshold may be different or contradictory, depending on its time, severity, and kind [9].
The aim of the study was to investigate the effect of three types of common stresses in modern living environment, i.e. electromagnetic waves, immobilization, and disturbance, individually and combined on pain threshold in infant male rats.
This study is an experimental one.
The research society was the population of pregnant female rats of Sprague Race (Razi Vaccine and Serum Research Center; Iran) and all their own male infants. All the rats were kept under proper light and temperature at Animal House of the University with unlimited available food and water.
40 female rats and all their own male infants were studied.
After confirmation of pregnancy with vaginal plug, the female rats were divided into 5 “control”, ”electromagnetic stress”, “immobilization stress”, “disturbance stress”, and “combined stress” groups. These groups, in the order they have been listed, show “normal pregnancy without stress”, “4 hours a day exposure of 1.2 t and 50 Hz electromagnetic waves”, “2 times a day 30 minutes immobilization stress”, “keeping all the group rats in a small cage”, and “combination of three stresses similar to each individual group’s stress”, respectively. From eighth day of gestation, pregnant rats of stress groups were exposed to stress for 10 consecutive days. To produce electromagnetic field, 2 solenoids with same dimensions and nearly 1780 rounds were used, being in serial connection to form a long solenoid of 3560 rounds. Animals’ placement point was in the middle of the solenoid. 75 days after childbirth (after maturity), the male infants were subjected to formalin pain test. Measuring the pain intensity was done via "zero" (putting the feet on the ground completely), "1" (putting the paw on the ground), "2" (raising the feet), and "3" (biting or licking the feet) scales, with every minute recording [10]. Data were analyzed by the use of SPSS 18 software, One-way Variance Analysis test (to general comparison), and Tukey's Post Hoc test (to compare the results between groups).
By subcutaneous injection of formalin into the plantar, acute and chronic pain stages were observed in the rats of all groups, which had no significant statistical difference. Average pain severity at the acute phase of the formalin test between each stress group and the control group was not significant. Average pain severity of the interphase stage of the formalin test was significant only between the electromagnetic stress and the control groups. Average pain severity at the chronic stage of formalin test, especially during 15 to 40 minutes, was significant between each of the combined stress and immobility stress groups on the one hand, and the control group on the other hand (Diagram 1).
Non-declared
Non-declared
Non-declared
Stress during pregnancy affects the pain behavior of the rats after maturity. In addition, it is probable that the impact of some combined stresses on chronic pain feeling and understanding system is more than that of stress alone does.
Researchers feel grateful to Research Deputy of Qazvin University of Medical Sciences, and Faculty of Paramedical Sciences.
Non-declared
Care of the rats was done according to the international ethical instructions on working with animals.
Research Deputy of Qazvin University of Medical Sciences and Faculty of Paramedical Sciences funded the research.
TABLES and CHARTS
Show attach fileCITIATION LINKS
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[2]Kofman O. The role of prenatal stress in the etiology of developmental behavioural disorders. Neurosci Biobehav Rev. 2002;26(4):457-70.
[3]Sadaghiani MM, Saboory E. Prenatal stress potentiates pilocarpine-induced epileptic behaviors in infant rats both time and sex dependently. Epil Behav. 2010;18(3):166-70. (http://www.sciencedirect.com/science/article/pii/S1525505010003100)
[4]Rangon CM, Fortes S, Lelièvre V, Leroux P, Plaisant F, Joubert C, Lanfumey L, Cohen-Salmon C, Gressens P. Chronic mild stress during gestation worsens neonatal brain lesions in mice. J Neurosci. 2007;27(28):7532-40. (http://www.jneurosci.org/content/27/28/7532.short)
[5]Hansen D, Lou HC, Nordentoft M, Pryds OA, Jensen FR, Nim J, Hemmingsen RP. The significance of psychosocial stress for pregnancy course and fetal development. Ugeskr Laeger. 1996;158(17):2369-72. (http://europepmc.org/abstract/MED/8685988/reload=0;jsessionid=gEAkppzB3mjtBqkANb3F.12)
[6]Slamberova R, Schindler CJ, Pometlova M, Urkuti C, Purow-Sokol JA, Vathy I. Prenatal morphine exposure alters learning and memory in male rats. Physiol Behav. 2001;73(1-2):93-103. (http://www.sciencedirect.com/science/article/pii/S0031938401004693)
[7]Chiou LC, Yeh GC, Fan SH, How CH, Chuang KC, Tao PL. Prenatal morphine exposure decreases analgesia but not K+ channel activation. Neuroreport. 2003;14(2):239-42. (http://journals.lww.com/neuroreport/Abstract/2003/02100/Prenatal_morphine_exposure_decreases_analgesia_but.16.aspx)
[8]Sarkaki A, Heydari A, Shahraki M. The effect of noise stress during fetal life on pain in rats. J Kerman Uni Med Sci. 2000;7(2):53-9. (http://webamooz.kmu.ac.ir/en/index.php/kmus/article/view/344)
[9]Butkevich IP, Vershinina EA. Prenatal stress alters time characteristics and intensity of formalin-induced pain responses in juvenile rats. Brain Res. 2001;915(1):88-93. (http://www.sciencedirect.com/science/article/pii/S0006899301028190)
[10]Azhdari Zarmehri H, Semnanian S, Fathollahi Y, Erami E, Khakpay R, Azizi H, et al. Intra-periaqueductal gray matter microinjection of orexin-A decreases formalin-induced nociceptive behaviors in adult male rats. J Pain. 2011;12(2):280-7. (http://www.sciencedirect.com/science/article/pii/S1526590010007431)
[11]Dray A, urban L. New pharmacological strategies for pain relief. Ann Rev Pharmacol Toxicol. 1996;36(1):253-80. (http://www.annualreviews.org/doi/abs/10.1146/annurev.pa.36.040196.001345?journalCode=pharmtox)
[12]Porro CA, Cavazzuti M. Spatial and temporal aspects of spinal cord and brainstem activation in the formalin pain model. Prog Neurobiol. 1993;41(5):565-07. (http://www.sciencedirect.com/science/article/pii/030100829390044S)
[13]Puig S, Rivot JP, Benson JM. Effect of subcutaneous administration of the chemical halogen formalin, on 5-HT metabolism in the nucleus raphe Magnus and freely moving rats. Brain Res. 1992;36(5):112-24. (http://www.sciencedirect.com/science/article/pii/000689939291102K)
[14]Yanga J, Lia W, Liub X, Lia Z, Lib H, Yangb G, et al. Enriched environment treatment counteracts enhanced addictive and depressive-like behavior induced by prenatal chronic stress. Brain Res. 2006;1125(1):132-7. (http://www.sciencedirect.com/science/article/pii/S0006899306030745)
[15]Cagiano R, De Salvia MA, Perischella M, Renna G, Tattoli M, Cuomo V. Behavioural changes in the offspring of rats exposed to diazepam during gestation. Eur J Pharmacol. 1990;177(1):67-4.
[16]Cannizzaro C, Cannizzaro E, Gagliano M, Mangiapane N. Behavioural responsiveness to picrotoxin and desipramine in adult rats prenatally exposed to different benzodiazepine receptor agonists. Neuropsychopharmacol. 1995;5(4):523-6.
[17]Pivina SG, Shamolina TS, Akulova VK, Ordian NE. Sensitiveness to social stress in female rats with alteration of the pituitary-adrenal axis stress reactivity. Ross Fiziol Zh IM Sechenova. 2007;93(11):1319-25.
[18]Nazari Z, Sahraei H, Sadoughi M. The effect of chronic stress in pregnant mothers on the responsiveness to morphine in mice: a behavioral sensitization study. Yafteh. 2008;10(3):47-56.
[19]Fujioka T, Sakata Y, Yaamaguchi K, Shibasaki T, Kato H, Nakamura S. The effects of prenanatal stress the development of hypothalamicparaventricular neurons in fetal rats. Neuroscience. 1999;92(3):1079-88.
[20]Kademian S, Pérez MF, Keller EA. Perinatal undernutrition: changes in brain opiate receptor density. Nutr Neurosci. 2002;5(1):53-7.
[21]Huizink AC, Mulder EJ, Buitelaar JK. Prenatal stress and risk for psychopathology: specific effects or induction of general susceptibility. Psychol Bulletin. 2004;130(1):115-42.
[22]Shahraki MR, MirShekari H, Palan MJ. The comparison of nociceptive effect of Teucrium polium and morphine in female rats. Horizon Med Sci. 2006;12(1):10-4.
[23]Heine S, Michalakis S, Kallenborn GW, Lu R, Lim HY, Weiland J, et al. CNGA3: a target of spinal nitric oxide/cGMP signaling and modulator of inflammatory pain hypersensitivity. J Neurosci. 2011;31(31):11184-92.
[24]Tegeder I, Scheving R, Wittig I, Geisslinger G. SNO-ing at the nociceptive synapse? Pharmacol Rev. 2011;63(2):366-89.
[25]Geisler S, Bérod A, Zahm DS, Rostène W. Brain neurotensin, psychostimulants, and stress: emphasis on neuroanatomical substrates. Elsevier pept. 2006;27(10):2364-84.
[26]Celikozlu SD, Ozyurt MS, Cimbiz A, Yardimoglu MY, Cayci MK, Ozay Y. The effects of long-term exposure of magnetic field via 900-MHz GSM radiation on some biochemical parameters and brain histology in rats. Electromagnetic Biol Med. 2012;31(4):344-55.
[27]Zare S, Hayatgeibi H, Alivandi S, Ebadi AG. Effects of whole-body magnetic field on changes of glucose and cortisol hormone in guinea pigs. Am J Biochem Biotechnol. 2005;1(4): 217-9.
[2]Kofman O. The role of prenatal stress in the etiology of developmental behavioural disorders. Neurosci Biobehav Rev. 2002;26(4):457-70.
[3]Sadaghiani MM, Saboory E. Prenatal stress potentiates pilocarpine-induced epileptic behaviors in infant rats both time and sex dependently. Epil Behav. 2010;18(3):166-70. (http://www.sciencedirect.com/science/article/pii/S1525505010003100)
[4]Rangon CM, Fortes S, Lelièvre V, Leroux P, Plaisant F, Joubert C, Lanfumey L, Cohen-Salmon C, Gressens P. Chronic mild stress during gestation worsens neonatal brain lesions in mice. J Neurosci. 2007;27(28):7532-40. (http://www.jneurosci.org/content/27/28/7532.short)
[5]Hansen D, Lou HC, Nordentoft M, Pryds OA, Jensen FR, Nim J, Hemmingsen RP. The significance of psychosocial stress for pregnancy course and fetal development. Ugeskr Laeger. 1996;158(17):2369-72. (http://europepmc.org/abstract/MED/8685988/reload=0;jsessionid=gEAkppzB3mjtBqkANb3F.12)
[6]Slamberova R, Schindler CJ, Pometlova M, Urkuti C, Purow-Sokol JA, Vathy I. Prenatal morphine exposure alters learning and memory in male rats. Physiol Behav. 2001;73(1-2):93-103. (http://www.sciencedirect.com/science/article/pii/S0031938401004693)
[7]Chiou LC, Yeh GC, Fan SH, How CH, Chuang KC, Tao PL. Prenatal morphine exposure decreases analgesia but not K+ channel activation. Neuroreport. 2003;14(2):239-42. (http://journals.lww.com/neuroreport/Abstract/2003/02100/Prenatal_morphine_exposure_decreases_analgesia_but.16.aspx)
[8]Sarkaki A, Heydari A, Shahraki M. The effect of noise stress during fetal life on pain in rats. J Kerman Uni Med Sci. 2000;7(2):53-9. (http://webamooz.kmu.ac.ir/en/index.php/kmus/article/view/344)
[9]Butkevich IP, Vershinina EA. Prenatal stress alters time characteristics and intensity of formalin-induced pain responses in juvenile rats. Brain Res. 2001;915(1):88-93. (http://www.sciencedirect.com/science/article/pii/S0006899301028190)
[10]Azhdari Zarmehri H, Semnanian S, Fathollahi Y, Erami E, Khakpay R, Azizi H, et al. Intra-periaqueductal gray matter microinjection of orexin-A decreases formalin-induced nociceptive behaviors in adult male rats. J Pain. 2011;12(2):280-7. (http://www.sciencedirect.com/science/article/pii/S1526590010007431)
[11]Dray A, urban L. New pharmacological strategies for pain relief. Ann Rev Pharmacol Toxicol. 1996;36(1):253-80. (http://www.annualreviews.org/doi/abs/10.1146/annurev.pa.36.040196.001345?journalCode=pharmtox)
[12]Porro CA, Cavazzuti M. Spatial and temporal aspects of spinal cord and brainstem activation in the formalin pain model. Prog Neurobiol. 1993;41(5):565-07. (http://www.sciencedirect.com/science/article/pii/030100829390044S)
[13]Puig S, Rivot JP, Benson JM. Effect of subcutaneous administration of the chemical halogen formalin, on 5-HT metabolism in the nucleus raphe Magnus and freely moving rats. Brain Res. 1992;36(5):112-24. (http://www.sciencedirect.com/science/article/pii/000689939291102K)
[14]Yanga J, Lia W, Liub X, Lia Z, Lib H, Yangb G, et al. Enriched environment treatment counteracts enhanced addictive and depressive-like behavior induced by prenatal chronic stress. Brain Res. 2006;1125(1):132-7. (http://www.sciencedirect.com/science/article/pii/S0006899306030745)
[15]Cagiano R, De Salvia MA, Perischella M, Renna G, Tattoli M, Cuomo V. Behavioural changes in the offspring of rats exposed to diazepam during gestation. Eur J Pharmacol. 1990;177(1):67-4.
[16]Cannizzaro C, Cannizzaro E, Gagliano M, Mangiapane N. Behavioural responsiveness to picrotoxin and desipramine in adult rats prenatally exposed to different benzodiazepine receptor agonists. Neuropsychopharmacol. 1995;5(4):523-6.
[17]Pivina SG, Shamolina TS, Akulova VK, Ordian NE. Sensitiveness to social stress in female rats with alteration of the pituitary-adrenal axis stress reactivity. Ross Fiziol Zh IM Sechenova. 2007;93(11):1319-25.
[18]Nazari Z, Sahraei H, Sadoughi M. The effect of chronic stress in pregnant mothers on the responsiveness to morphine in mice: a behavioral sensitization study. Yafteh. 2008;10(3):47-56.
[19]Fujioka T, Sakata Y, Yaamaguchi K, Shibasaki T, Kato H, Nakamura S. The effects of prenanatal stress the development of hypothalamicparaventricular neurons in fetal rats. Neuroscience. 1999;92(3):1079-88.
[20]Kademian S, Pérez MF, Keller EA. Perinatal undernutrition: changes in brain opiate receptor density. Nutr Neurosci. 2002;5(1):53-7.
[21]Huizink AC, Mulder EJ, Buitelaar JK. Prenatal stress and risk for psychopathology: specific effects or induction of general susceptibility. Psychol Bulletin. 2004;130(1):115-42.
[22]Shahraki MR, MirShekari H, Palan MJ. The comparison of nociceptive effect of Teucrium polium and morphine in female rats. Horizon Med Sci. 2006;12(1):10-4.
[23]Heine S, Michalakis S, Kallenborn GW, Lu R, Lim HY, Weiland J, et al. CNGA3: a target of spinal nitric oxide/cGMP signaling and modulator of inflammatory pain hypersensitivity. J Neurosci. 2011;31(31):11184-92.
[24]Tegeder I, Scheving R, Wittig I, Geisslinger G. SNO-ing at the nociceptive synapse? Pharmacol Rev. 2011;63(2):366-89.
[25]Geisler S, Bérod A, Zahm DS, Rostène W. Brain neurotensin, psychostimulants, and stress: emphasis on neuroanatomical substrates. Elsevier pept. 2006;27(10):2364-84.
[26]Celikozlu SD, Ozyurt MS, Cimbiz A, Yardimoglu MY, Cayci MK, Ozay Y. The effects of long-term exposure of magnetic field via 900-MHz GSM radiation on some biochemical parameters and brain histology in rats. Electromagnetic Biol Med. 2012;31(4):344-55.
[27]Zare S, Hayatgeibi H, Alivandi S, Ebadi AG. Effects of whole-body magnetic field on changes of glucose and cortisol hormone in guinea pigs. Am J Biochem Biotechnol. 2005;1(4): 217-9.