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Nikkhouy, P., Abbasnejad, M., Esmaeili-Mahani, S., & Kooshki, R. (2024). Mode of delivery alters sensitivity to thermal and chemical stimuli in adult rats: An experimental study. International Journal of Reproductive BioMedicine (IJRM), 22(2), 101–110. https://doi.org/10.18502/ijrm.v22i2.15707
https://doi.org/10.18502/ijrm.v22i2.15707
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authors
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Parastoo Nikkhouy
Parastoo Nikkhouy
Department of Biology, Faculty of Sciences, Shahid Bahonar University of Kerman, Kerman, Iran.
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Mehdi Abbasnejad
Mehdi Abbasnejad
Department of Biology, Faculty of Sciences, Shahid Bahonar University of Kerman, Kerman, Iran.
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Saeed Esmaeili-Mahani
Saeed Esmaeili-Mahani
Department of Biology, Faculty of Sciences, Shahid Bahonar University of Kerman, Kerman, Iran.
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Razieh Kooshki
Razieh Kooshki
Department of Biology, Faculty of Sciences, Lorestan University, Khorramabad, Iran.
Published Date
- Mar 25, 2024
Mode of delivery alters sensitivity to thermal and chemical stimuli in adult rats: An experimental study
Abstract
Background: The mode of delivery might prompt a long-lasting alteration in physiological and behavioral responsiveness in offspring.
Objective: This study was intended to evaluate if the mode of delivery could alter sensitivity to thermal and chemical stimuli in female rats.
Materials and Methods: 56 adult female Wistar rats (200–220 gr) that were born by vaginal or cesarean section (C-section) were used (n = 28/each). Inflammatory pain was induced by subcutaneous injection of formalin into the hind paw. The thermal nociceptive threshold was determined by tail-flick and hot plate tests. Besides, the Western blot test was used to evaluate the spinal cord levels of c-Fos and c-Jun proteins.
Results: Formalin-induced inflammation was significantly decreased in C-section group as compared to vaginally born rats (p < 0.001). The baseline nociceptive threshed and morphine-induced analgesia were significantly increased in C-section groups in comparison to vaginally born rats. In addition, the levels of c-Fos and c-Jun proteins were significantly decreased in the spinal cord of C-section rats as compared to vaginally born animals (p < 0.01). Morphine treatment could decrease the expression of c-Fos and c-Jun in the C-section group (p < 0.05).
Conclusion: Overall, C-section rats showed lower spinal nociceptive processing and neuronal activity later in life, compared to the vaginal born rats.
Key words: Childbirth, C-section, Nociception, Inflammation, Rats.
References
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[15] Deuis J, Dvorakova LS, Vetter I. Methods used to evaluate pain behaviors in rodents. Front Mol Neurosci 2017; 10: 284.
[16] Sule R, Rivera G, Gomes AV. Western blotting (immunoblotting): History, theory, uses, protocol and problems. Biotechniques 2023; 75: 99–114.
[17] Bergqvist LL, Katz-Salamon M, Hertegård S, Anand K, Lagercrantz H. Mode of delivery modulates physiological and behavioral responses to neonatal pain. J Perinatol 2009; 29: 44–50.
[18] Ferreira EAL, Nassif DS, Silva MJD, Barbosa SMdM, Módolo NSP, Barros GAM. [Evaluation of pain in vaginal and caesarean section birth newborns before and after intramuscular injection]. Braz J Pain 2020; 3: 123–126. (in Brazilian)
[19] Schuller Ch, Känel N, Müller O, Kind AB, Tinner EM, Hösli I, et al. Stress and pain response of neonates after spontaneous birth and vacuum-assisted and cesarean delivery. Am J Obstet Gynecol 2012; 207: 416.
[20] Glover V, O’connor T, O’Donnell K. Prenatal stress and the programming of the HPA axis. Neurosci Biobehav Rev 2010; 35: 17–22.
[21] Kaviany Nejad R, Goodarzi MT, Shfiee Gh, Pezeshki N, Sohrabi M. Comparison of oxidative stress markers and serum cortisol between normal labor and selective cesarean section born neonates. J Clin Diagn Res 2016; 10: BC01.
[22] Cabré S, Ratsika A, Rea K, Stanton C, Cryan JF. Animal models for assessing impact of C-section delivery on biological systems. Neurosci Biobehav Rev 2022; 135: 104555.
[23] Chiesa M, Ferrari DC, Ben-Ari Y. Alteration in the time and/or mode of delivery differentially modulates early development in mice. Mol Brain 2020; 13: 34.
[24] Gao Y-J, Ji R-R. c-Fos and pERK, which is a better marker for neuronal activation and central sensitization after noxious stimulation and tissue injury? Open Pain J 2009; 2: 11–17.
[25] Ikeda K, Onimaru H, Matsuura T, Kawakami K. Different impacts on brain function depending on the mode of delivery. Brain Res 2019; 1720: 146289.
[26] Malamitsi-Puchner A, Protonotariou E, Boutsikou T, Makrakis E, Sarandakou A, Creatsas G. The influence of the mode of delivery on circulating cytokine concentrations in the perinatal period. Early Hum Dev 2005; 81: 387–392.
[27] Palm M, Axelsson O, Wernroth L, Larsson A, Basu S. Involvement of inflammation in normal pregnancy. Acta Obstet Gynecol Scand 2013; 92: 601–605.
[28] Diaz J, Abiola S, Kim N, Avaritt O, Flock D, Yu J, et al. Therapeutic hypothermia provides variable protection against behavioral deficits after neonatal hypoxiaischemia: A potential role for brain-derived neurotrophic factor. Dev Neurosci 2017; 39: 257–272.
[29] Ayres-de-Campos D. Acute fetal hypoxia/acidosis. In: Ayres-de-Campos D. Obstetric emergencies: A practical guide. Portugal: Springer; 2017. 7–25.
[30] Panfoli I, Candiano G, Malova M, De Angelis L, Cardiello V, Buonocore G, et al. Oxidative stress as a primary risk factor for brain damage in preterm newborns. Front Pediatr 2018; 6: 369.
[31] Ilari S, Giancotti LA, Lauro F, Gliozzi M, Malafoglia V, Palma E, et al. Natural antioxidant control of neuropathic pain-exploring the role of mitochondrial SIRT3 pathway. Antioxidants 2020; 9: 1103.
[32] Sharma A, Kumar A. Role of antioxidant therapy for pain relief in chronic pancreatitis: Finding the signal in the noise. JGH Open 2021; 5: 327.
[33] Kaushik AS, Strath LJ, Sorge RE. Dietary interventions for treatment of chronic pain: Oxidative stress and inflammation. Pain Ther 2020; 9: 487–498.
[2] Chen H, Tan D. Cesarean section or natural childbirth? Cesarean birth may damage your health. Front Psychol 2019; 10: 351.
[3] Barba-Müller E, Craddock S, Carmona S, Hoekzema E. Brain plasticity in pregnancy and the postpartum period: Links to maternal caregiving and mental health. Arch Womens Ment Health 2019; 22: 289–299.
[4] Vasung L, Turk EA, Ferradal SL, Sutin J, Stout JN, Ahtam B, et al. Exploring early human brain development with structural and physiological neuroimaging. NeuroImage 2019; 187: 226–254.
[5] Fenton BW, Shih E, Zolton J. The neurobiology of pain perception in normal and persistent pain. Pain Manag 2015; 5: 297–317.
[6] Dahlquist K, Stuart A, Källén K. Planned cesarean section vs planned vaginal delivery among women without formal medical indication for planned cesarean section: A retrospective cohort study of maternal short−term complications. Acta Obstet Gynecol Scand 2022; 101: 1026–1032.
[7] Kristensen K, Henriksen L. Cesarean section and disease associated with immune function. J Allergy Clin Immunol 2016; 137: 587–590.
[8] Flick RP, Lee K, Hofer RE, Beinborn CW, Hambel EM, Klein MK, et al. Neuraxial labor analgesia for vaginal delivery and its effects on childhood learning disabilities. Anesth Analg 2011; 112: 1424–1431.
[9] Mohamadi-Jorjafki E, Abbasnejad M, Kooshki R, Esmaeili-Mahani S, Raoof M. Mode of delivery alters dental pulp nociception and pain-induced changes in cognitive performance in adults male rats. Can J Physiol Pharmacol 2020; 98: 717–724.
[10] Tork Zahrani S, Heshmat F, Abbasinia H, Delshad H, Shakeri N, Valiani M. The relationship between delivery mode and cord blood betaendorphins values in the newborns of nulliparous women. Arc Hygiene Sci 2021; 10: 235–242.
[11] Li Sh, Ye F, Farber JP, Linderoth B, Zhang T, Gu JW, et al. Dependence of c-fos expression on amplitude of high-frequency spinal cord stimulation in a rodent model. Neuromodulation 2019; 22: 272–278.
[12] Li Y-L, Chang X-R, Ma J-T, Zhao X, Yin L-T, Yan L-J, et al. Activation of peripheral group III metabotropic glutamate receptors suppressed formalin−induced nociception. Clin Exp Pharmacol Physiol 2022; 49: 319–326.
[13] Zhou F, Zhang W, Zhou J, Li M, Zhong F, Zhang Y, et al. Involvement of endoplasmic reticulum stress in formalininduced pain is attenuated by 4-phenylbutyric acid. J Pain Res 2017; 10: 653–662.
[14] Askari-Zahabi Kh, Abbasnejad M, Kooshki R, Raoof M, Esmaeili-Mahani S, Pourrahimi AM, et al. The role of basolateral amygdala orexin 1 receptors on the modulation of pain and psychosocial deficits in nitroglycerin-induced migraine model in adult male rats. Korean J Pain 2022; 35: 22–32.
[15] Deuis J, Dvorakova LS, Vetter I. Methods used to evaluate pain behaviors in rodents. Front Mol Neurosci 2017; 10: 284.
[16] Sule R, Rivera G, Gomes AV. Western blotting (immunoblotting): History, theory, uses, protocol and problems. Biotechniques 2023; 75: 99–114.
[17] Bergqvist LL, Katz-Salamon M, Hertegård S, Anand K, Lagercrantz H. Mode of delivery modulates physiological and behavioral responses to neonatal pain. J Perinatol 2009; 29: 44–50.
[18] Ferreira EAL, Nassif DS, Silva MJD, Barbosa SMdM, Módolo NSP, Barros GAM. [Evaluation of pain in vaginal and caesarean section birth newborns before and after intramuscular injection]. Braz J Pain 2020; 3: 123–126. (in Brazilian)
[19] Schuller Ch, Känel N, Müller O, Kind AB, Tinner EM, Hösli I, et al. Stress and pain response of neonates after spontaneous birth and vacuum-assisted and cesarean delivery. Am J Obstet Gynecol 2012; 207: 416.
[20] Glover V, O’connor T, O’Donnell K. Prenatal stress and the programming of the HPA axis. Neurosci Biobehav Rev 2010; 35: 17–22.
[21] Kaviany Nejad R, Goodarzi MT, Shfiee Gh, Pezeshki N, Sohrabi M. Comparison of oxidative stress markers and serum cortisol between normal labor and selective cesarean section born neonates. J Clin Diagn Res 2016; 10: BC01.
[22] Cabré S, Ratsika A, Rea K, Stanton C, Cryan JF. Animal models for assessing impact of C-section delivery on biological systems. Neurosci Biobehav Rev 2022; 135: 104555.
[23] Chiesa M, Ferrari DC, Ben-Ari Y. Alteration in the time and/or mode of delivery differentially modulates early development in mice. Mol Brain 2020; 13: 34.
[24] Gao Y-J, Ji R-R. c-Fos and pERK, which is a better marker for neuronal activation and central sensitization after noxious stimulation and tissue injury? Open Pain J 2009; 2: 11–17.
[25] Ikeda K, Onimaru H, Matsuura T, Kawakami K. Different impacts on brain function depending on the mode of delivery. Brain Res 2019; 1720: 146289.
[26] Malamitsi-Puchner A, Protonotariou E, Boutsikou T, Makrakis E, Sarandakou A, Creatsas G. The influence of the mode of delivery on circulating cytokine concentrations in the perinatal period. Early Hum Dev 2005; 81: 387–392.
[27] Palm M, Axelsson O, Wernroth L, Larsson A, Basu S. Involvement of inflammation in normal pregnancy. Acta Obstet Gynecol Scand 2013; 92: 601–605.
[28] Diaz J, Abiola S, Kim N, Avaritt O, Flock D, Yu J, et al. Therapeutic hypothermia provides variable protection against behavioral deficits after neonatal hypoxiaischemia: A potential role for brain-derived neurotrophic factor. Dev Neurosci 2017; 39: 257–272.
[29] Ayres-de-Campos D. Acute fetal hypoxia/acidosis. In: Ayres-de-Campos D. Obstetric emergencies: A practical guide. Portugal: Springer; 2017. 7–25.
[30] Panfoli I, Candiano G, Malova M, De Angelis L, Cardiello V, Buonocore G, et al. Oxidative stress as a primary risk factor for brain damage in preterm newborns. Front Pediatr 2018; 6: 369.
[31] Ilari S, Giancotti LA, Lauro F, Gliozzi M, Malafoglia V, Palma E, et al. Natural antioxidant control of neuropathic pain-exploring the role of mitochondrial SIRT3 pathway. Antioxidants 2020; 9: 1103.
[32] Sharma A, Kumar A. Role of antioxidant therapy for pain relief in chronic pancreatitis: Finding the signal in the noise. JGH Open 2021; 5: 327.
[33] Kaushik AS, Strath LJ, Sorge RE. Dietary interventions for treatment of chronic pain: Oxidative stress and inflammation. Pain Ther 2020; 9: 487–498.