Skip to main content
Top
Published in: Molecular Pain 1/2015

Open Access 01-12-2015 | Research

Short-term pre- and post-operative stress prolongs incision-induced pain hypersensitivity without changing basal pain perception

Authors: Jing Cao, Po-Kai Wang, Vinod Tiwari, Lingli Liang, Brianna Marie Lutz, Kun-Ruey Shieh, Wei-Dong Zang, Andrew G. Kaufman, Alex Bekker, Xiao-Qun Gao, Yuan-Xiang Tao

Published in: Molecular Pain | Issue 1/2015

Login to get access

Abstract

Background

Chronic stress has been reported to increase basal pain sensitivity and/or exacerbate existing persistent pain. However, most surgical patients have normal physiological and psychological health status such as normal pain perception before surgery although they do experience short-term stress during pre- and post-operative periods. Whether or not this short-term stress affects persistent postsurgical pain is unclear.

Results

In this study, we showed that pre- or post-surgical exposure to immobilization 6 h daily for three consecutive days did not change basal responses to mechanical, thermal, or cold stimuli or peak levels of incision-induced hypersensitivity to these stimuli; however, immobilization did prolong the duration of incision-induced hypersensitivity in both male and female rats. These phenomena were also observed in post-surgical exposure to forced swimming 25 min daily for 3 consecutive days. Short-term stress induced by immobilization was demonstrated by an elevation in the level of serum corticosterone, an increase in swim immobility, and a decrease in sucrose consumption. Blocking this short-term stress via intrathecal administration of a selective glucocorticoid receptor antagonist, RU38486, or bilateral adrenalectomy significantly attenuated the prolongation of incision-induced hypersensitivity to mechanical, thermal, and cold stimuli.

Conclusion

Our results indicate that short-term stress during the pre- or post-operative period delays postoperative pain recovery although it does not affect basal pain perception. Prevention of short-term stress may facilitate patients’ recovery from postoperative pain.
Literature
1.
go back to reference Cregg R, Anwar S, Farquhar-Smith P. Persistent postsurgical pain. Curr Opin Support Palliat Care. 2013;7:144–52.CrossRefPubMed Cregg R, Anwar S, Farquhar-Smith P. Persistent postsurgical pain. Curr Opin Support Palliat Care. 2013;7:144–52.CrossRefPubMed
3.
go back to reference Angst MS. Intraoperative use of remifentanil for TIVA: postoperative pain, acute tolerance, and opioid-induced hyperalgesia. J Cardiothorac Vasc Anesth. 2015;29(Suppl 1):S16–S22.CrossRefPubMed Angst MS. Intraoperative use of remifentanil for TIVA: postoperative pain, acute tolerance, and opioid-induced hyperalgesia. J Cardiothorac Vasc Anesth. 2015;29(Suppl 1):S16–S22.CrossRefPubMed
5.
go back to reference Mamie C, Bernstein M, Morabia A, Klopfenstein CE, Sloutskis D, Forster A. Are there reliable predictors of postoperative pain? Acta Anaesthesiol Scand. 2004;48:234–42.CrossRefPubMed Mamie C, Bernstein M, Morabia A, Klopfenstein CE, Sloutskis D, Forster A. Are there reliable predictors of postoperative pain? Acta Anaesthesiol Scand. 2004;48:234–42.CrossRefPubMed
6.
go back to reference Kundermann B, Spernal J, Huber MT, Krieg JC, Lautenbacher S. Sleep deprivation affects thermal pain thresholds but not somatosensory thresholds in healthy volunteers. Psychosom Med. 2004;66:932–7.CrossRefPubMed Kundermann B, Spernal J, Huber MT, Krieg JC, Lautenbacher S. Sleep deprivation affects thermal pain thresholds but not somatosensory thresholds in healthy volunteers. Psychosom Med. 2004;66:932–7.CrossRefPubMed
7.
go back to reference Roehrs T, Hyde M, Blaisdell B, Greenwald M, Roth T. Sleep loss and REM sleep loss are hyperalgesic. Sleep. 2006;29:145–51.PubMed Roehrs T, Hyde M, Blaisdell B, Greenwald M, Roth T. Sleep loss and REM sleep loss are hyperalgesic. Sleep. 2006;29:145–51.PubMed
8.
go back to reference Huang CT, Chiang RP, Chen CL, Tsai YJ. Sleep deprivation aggravates median nerve injury-induced neuropathic pain and enhances microglial activation by suppressing melatonin secretion. Sleep. 2014;37:1513–23.PubMedCentralPubMed Huang CT, Chiang RP, Chen CL, Tsai YJ. Sleep deprivation aggravates median nerve injury-induced neuropathic pain and enhances microglial activation by suppressing melatonin secretion. Sleep. 2014;37:1513–23.PubMedCentralPubMed
9.
go back to reference Raymond I, Nielsen TA, Lavigne G, Manzini C, Choiniere M. Quality of sleep and its daily relationship to pain intensity in hospitalized adult burn patients. Pain. 2001;92:381–8.CrossRefPubMed Raymond I, Nielsen TA, Lavigne G, Manzini C, Choiniere M. Quality of sleep and its daily relationship to pain intensity in hospitalized adult burn patients. Pain. 2001;92:381–8.CrossRefPubMed
10.
go back to reference Alexander JK, DeVries AC, Kigerl KA, Dahlman JM, Popovich PG. Stress exacerbates neuropathic pain via glucocorticoid and NMDA receptor activation. Brain Behav Immun. 2009;23:851–60.PubMedCentralCrossRefPubMed Alexander JK, DeVries AC, Kigerl KA, Dahlman JM, Popovich PG. Stress exacerbates neuropathic pain via glucocorticoid and NMDA receptor activation. Brain Behav Immun. 2009;23:851–60.PubMedCentralCrossRefPubMed
11.
go back to reference Lautenbacher S, Kundermann B, Krieg JC. Sleep deprivation and pain perception. Sleep Med Rev. 2006;10:357–69.CrossRefPubMed Lautenbacher S, Kundermann B, Krieg JC. Sleep deprivation and pain perception. Sleep Med Rev. 2006;10:357–69.CrossRefPubMed
12.
go back to reference Kamdar BB, Needham DM, Collop NA. Sleep deprivation in critical illness: its role in physical and psychological recovery. J Intensive Care Med. 2012;27:97–111.PubMedCentralCrossRefPubMed Kamdar BB, Needham DM, Collop NA. Sleep deprivation in critical illness: its role in physical and psychological recovery. J Intensive Care Med. 2012;27:97–111.PubMedCentralCrossRefPubMed
13.
go back to reference Onen SH, Alloui A, Gross A, Eschallier A, Dubray C. The effects of total sleep deprivation, selective sleep interruption and sleep recovery on pain tolerance thresholds in healthy subjects. J Sleep Res. 2001;10:35–42.CrossRefPubMed Onen SH, Alloui A, Gross A, Eschallier A, Dubray C. The effects of total sleep deprivation, selective sleep interruption and sleep recovery on pain tolerance thresholds in healthy subjects. J Sleep Res. 2001;10:35–42.CrossRefPubMed
14.
go back to reference Wang PK, Cao J, Wang H, Liang L, Zhang J, Lutz BM, Shieh KR, Bekker A, Tao YX. Short-term sleep disturbance-induced stress does not affect basal pain perception, but does delay postsurgical pain recovery. J Pain. 2015;16:1186–99.CrossRefPubMed Wang PK, Cao J, Wang H, Liang L, Zhang J, Lutz BM, Shieh KR, Bekker A, Tao YX. Short-term sleep disturbance-induced stress does not affect basal pain perception, but does delay postsurgical pain recovery. J Pain. 2015;16:1186–99.CrossRefPubMed
15.
go back to reference Liu X, Serova L, Kvetnansky R, Sabban EL. Identifying the stress transcriptome in the adrenal medulla following acute and repeated immobilization. Ann N Y Acad Sci. 2008;1148:1–28.PubMedCentralCrossRefPubMed Liu X, Serova L, Kvetnansky R, Sabban EL. Identifying the stress transcriptome in the adrenal medulla following acute and repeated immobilization. Ann N Y Acad Sci. 2008;1148:1–28.PubMedCentralCrossRefPubMed
16.
go back to reference Nankova B, Kvetnansky R, McMahon A, Viskupic E, Hiremagalur B, Frankle G, et al. Induction of tyrosine hydroxylase gene expression by a nonneuronal nonpituitary-mediated mechanism in immobilization stress. Proc Natl Acad Sci USA. 1994;91:5937–41.PubMedCentralCrossRefPubMed Nankova B, Kvetnansky R, McMahon A, Viskupic E, Hiremagalur B, Frankle G, et al. Induction of tyrosine hydroxylase gene expression by a nonneuronal nonpituitary-mediated mechanism in immobilization stress. Proc Natl Acad Sci USA. 1994;91:5937–41.PubMedCentralCrossRefPubMed
17.
go back to reference Leggio GM, Micale V, Drago F. Increased sensitivity to antidepressants of D3 dopamine receptor-deficient mice in the forced swim test (FST). Eur Neuropsychopharmacol. 2008;18:271–7.CrossRefPubMed Leggio GM, Micale V, Drago F. Increased sensitivity to antidepressants of D3 dopamine receptor-deficient mice in the forced swim test (FST). Eur Neuropsychopharmacol. 2008;18:271–7.CrossRefPubMed
18.
go back to reference Brennan TJ, Vandermeulen EP, Gebhart GF. Characterization of a rat model of incisional pain. Pain. 1996;64:493–501.CrossRefPubMed Brennan TJ, Vandermeulen EP, Gebhart GF. Characterization of a rat model of incisional pain. Pain. 1996;64:493–501.CrossRefPubMed
19.
go back to reference Atianjoh FE, Yaster M, Zhao X, Takamiya K, Xia J, Gauda EB, et al. Spinal cord protein interacting with C kinase 1 is required for the maintenance of complete Freund’s adjuvant-induced inflammatory pain but not for incision-induced post-operative pain. Pain. 2010;151:226–34.PubMedCentralCrossRefPubMed Atianjoh FE, Yaster M, Zhao X, Takamiya K, Xia J, Gauda EB, et al. Spinal cord protein interacting with C kinase 1 is required for the maintenance of complete Freund’s adjuvant-induced inflammatory pain but not for incision-induced post-operative pain. Pain. 2010;151:226–34.PubMedCentralCrossRefPubMed
20.
go back to reference Chu YC, Chan KH, Tsou MY, Lin SM, Hsieh YC, Tao YX. Mechanical pain hypersensitivity after incisional surgery is enhanced in rats subjected to neonatal peripheral inflammation: effects of N-methyl-d-aspartate receptor antagonists. Anesthesiology. 2007;106:1204–12.CrossRefPubMed Chu YC, Chan KH, Tsou MY, Lin SM, Hsieh YC, Tao YX. Mechanical pain hypersensitivity after incisional surgery is enhanced in rats subjected to neonatal peripheral inflammation: effects of N-methyl-d-aspartate receptor antagonists. Anesthesiology. 2007;106:1204–12.CrossRefPubMed
22.
go back to reference Bell JR, Bernasochi GB, Varma U, Raaijmakers AJ, Delbridge LM. Sex and sex hormones in cardiac stress–mechanistic insights. J Steroid Biochem Mol Biol. 2013;137:124–35.CrossRefPubMed Bell JR, Bernasochi GB, Varma U, Raaijmakers AJ, Delbridge LM. Sex and sex hormones in cardiac stress–mechanistic insights. J Steroid Biochem Mol Biol. 2013;137:124–35.CrossRefPubMed
23.
go back to reference Willner P. Validity, reliability and utility of the chronic mild stress model of depression: a 10-year review and evaluation. Psychopharmacology. 1997;134:319–29.CrossRefPubMed Willner P. Validity, reliability and utility of the chronic mild stress model of depression: a 10-year review and evaluation. Psychopharmacology. 1997;134:319–29.CrossRefPubMed
24.
go back to reference Evans SJ, Moore FL, Murray TF. Solubilization and pharmacological characterization of a glucocorticoid membrane receptor from a amphibian brain. J Steroid Biochem Mol Biol. 1988;67:1–8.CrossRef Evans SJ, Moore FL, Murray TF. Solubilization and pharmacological characterization of a glucocorticoid membrane receptor from a amphibian brain. J Steroid Biochem Mol Biol. 1988;67:1–8.CrossRef
25.
go back to reference Wang S, Lim G, Zeng Q, Sung B, Yang L, Mao J. Central glucocorticoid receptors modulate the expression and function of spinal NMDA receptors after peripheral nerve injury. J Neurosci. 2005;25:488–95.CrossRefPubMed Wang S, Lim G, Zeng Q, Sung B, Yang L, Mao J. Central glucocorticoid receptors modulate the expression and function of spinal NMDA receptors after peripheral nerve injury. J Neurosci. 2005;25:488–95.CrossRefPubMed
26.
go back to reference Villagra NT, Berciano J, Altable M, Navascues J, Casafont I, Lafarga M, et al. PML bodies in reactive sensory ganglion neurons of the Guillain-Barre-syndrome. Neurobiol Dis. 2004;16:158–68.CrossRefPubMed Villagra NT, Berciano J, Altable M, Navascues J, Casafont I, Lafarga M, et al. PML bodies in reactive sensory ganglion neurons of the Guillain-Barre-syndrome. Neurobiol Dis. 2004;16:158–68.CrossRefPubMed
27.
go back to reference Condon J, Gosden C, Gardener D, Nickson P, Hewison M, Howie AJ, et al. Expression of type 2 11 beta-hyroxysteroid dehydrogenase and corticosteroid hormone receptors in early human fetal life. J Clin Endocrinol Metab. 1998;83:4490–7.PubMed Condon J, Gosden C, Gardener D, Nickson P, Hewison M, Howie AJ, et al. Expression of type 2 11 beta-hyroxysteroid dehydrogenase and corticosteroid hormone receptors in early human fetal life. J Clin Endocrinol Metab. 1998;83:4490–7.PubMed
28.
go back to reference Banik RK, Woo YC, Park SS, Brennan TJ. Strain and sex influence on pain sensitivity after plantar incision in the mouse. Anesthesiology. 2006;105:1246–53.CrossRefPubMed Banik RK, Woo YC, Park SS, Brennan TJ. Strain and sex influence on pain sensitivity after plantar incision in the mouse. Anesthesiology. 2006;105:1246–53.CrossRefPubMed
29.
go back to reference Hatakeyama S, Kawai Y, Ueyama T, Senba E. Nitric oxide synthase-containing magnocellular neurons of the rat hypothalamus synthesize oxytocin and vasopressin and express Fos following stress stimuli. J Chem Neuroanat. 1996;11:243–56.CrossRefPubMed Hatakeyama S, Kawai Y, Ueyama T, Senba E. Nitric oxide synthase-containing magnocellular neurons of the rat hypothalamus synthesize oxytocin and vasopressin and express Fos following stress stimuli. J Chem Neuroanat. 1996;11:243–56.CrossRefPubMed
30.
go back to reference Torres IL, Buffon A, Silveira PP, Duarte MZ, Bassani MG, Oliveira SS, et al. Effect of chronic and acute stress on ectonucleotidase activities in spinal cord. Physiol Behav. 2002;75:1–5.CrossRefPubMed Torres IL, Buffon A, Silveira PP, Duarte MZ, Bassani MG, Oliveira SS, et al. Effect of chronic and acute stress on ectonucleotidase activities in spinal cord. Physiol Behav. 2002;75:1–5.CrossRefPubMed
31.
go back to reference Jalalvand E, Javan M, Haeri-Rohani A, Ahmadiani A. Stress- and non-stress-mediated mechanisms are involved in pain-induced apoptosis in hippocampus and dorsal lumbar spinal cord in rats. Neuroscience. 2008;157:446–52.CrossRefPubMed Jalalvand E, Javan M, Haeri-Rohani A, Ahmadiani A. Stress- and non-stress-mediated mechanisms are involved in pain-induced apoptosis in hippocampus and dorsal lumbar spinal cord in rats. Neuroscience. 2008;157:446–52.CrossRefPubMed
32.
go back to reference Zahn PK, Brennan TJ. Lack of effect of intrathecally administered N-methyl-d-aspartate receptor antagonists in a rat model for postoperative pain. Anesthesiology. 1998;88:143–56.CrossRefPubMed Zahn PK, Brennan TJ. Lack of effect of intrathecally administered N-methyl-d-aspartate receptor antagonists in a rat model for postoperative pain. Anesthesiology. 1998;88:143–56.CrossRefPubMed
33.
go back to reference Pogatzki EM, Niemeier JS, Sorkin LS, Brennan TJ. Spinal glutamate receptor antagonists differentiate primary and secondary mechanical hyperalgesia caused by incision. Pain. 2003;105:97–107.CrossRefPubMed Pogatzki EM, Niemeier JS, Sorkin LS, Brennan TJ. Spinal glutamate receptor antagonists differentiate primary and secondary mechanical hyperalgesia caused by incision. Pain. 2003;105:97–107.CrossRefPubMed
34.
go back to reference Xu JT, Zhou X, Zhao X, Ligons D, Tiwari V, Lee CY, et al. Opioid receptor-triggered spinal mTORC1 activation contributes to morphine tolerance and hyperalgesia. J Clin Invest. 2014;124:592–603.PubMedCentralCrossRefPubMed Xu JT, Zhou X, Zhao X, Ligons D, Tiwari V, Lee CY, et al. Opioid receptor-triggered spinal mTORC1 activation contributes to morphine tolerance and hyperalgesia. J Clin Invest. 2014;124:592–603.PubMedCentralCrossRefPubMed
35.
go back to reference Rees SL, Panesar S, Steiner M, Fleming AS. The effects of adrenalectomy and corticosterone replacement on maternal behavior in the postpartum rat. Horm Behav. 2004;46:411–9.CrossRefPubMed Rees SL, Panesar S, Steiner M, Fleming AS. The effects of adrenalectomy and corticosterone replacement on maternal behavior in the postpartum rat. Horm Behav. 2004;46:411–9.CrossRefPubMed
36.
go back to reference Zhao X, Tang Z, Zhang H, Atianjoh FE, Zhao JY, Liang L, et al. A long noncoding RNA contributes to neuropathic pain by silencing Kcna2 in primary afferent neurons. Nat Neurosci. 2013;16:1024–31.PubMedCentralCrossRefPubMed Zhao X, Tang Z, Zhang H, Atianjoh FE, Zhao JY, Liang L, et al. A long noncoding RNA contributes to neuropathic pain by silencing Kcna2 in primary afferent neurons. Nat Neurosci. 2013;16:1024–31.PubMedCentralCrossRefPubMed
37.
go back to reference Chaplan SR, Bach FW, Pogrel JW, Chung JM, Yaksh TL. Quantitative assessment of tactile allodynia in the rat paw. J Neurosci Methods. 1994;53:55–63.CrossRefPubMed Chaplan SR, Bach FW, Pogrel JW, Chung JM, Yaksh TL. Quantitative assessment of tactile allodynia in the rat paw. J Neurosci Methods. 1994;53:55–63.CrossRefPubMed
38.
go back to reference Hui YH, Huang NH, Ebbert L, Bina H, Chiang A, Maples C, et al. Pharmacokinetic comparisons of tail-bleeding with cannula- or retro-orbital bleeding techniques in rats using six marketed drugs. J Pharmacol Toxicol Methods. 2007;56:256–64.CrossRefPubMed Hui YH, Huang NH, Ebbert L, Bina H, Chiang A, Maples C, et al. Pharmacokinetic comparisons of tail-bleeding with cannula- or retro-orbital bleeding techniques in rats using six marketed drugs. J Pharmacol Toxicol Methods. 2007;56:256–64.CrossRefPubMed
39.
go back to reference Sharma A, Fish BL, Moulder JE, Medhora M, Baker JE, Mader M, et al. Safety and blood sample volume and quality of a refined retro-orbital bleeding technique in rats using a lateral approach. Lab Anim (NY). 2014;43:63–6.CrossRef Sharma A, Fish BL, Moulder JE, Medhora M, Baker JE, Mader M, et al. Safety and blood sample volume and quality of a refined retro-orbital bleeding technique in rats using a lateral approach. Lab Anim (NY). 2014;43:63–6.CrossRef
Metadata
Title
Short-term pre- and post-operative stress prolongs incision-induced pain hypersensitivity without changing basal pain perception
Authors
Jing Cao
Po-Kai Wang
Vinod Tiwari
Lingli Liang
Brianna Marie Lutz
Kun-Ruey Shieh
Wei-Dong Zang
Andrew G. Kaufman
Alex Bekker
Xiao-Qun Gao
Yuan-Xiang Tao
Publication date
01-12-2015
Publisher
BioMed Central
Published in
Molecular Pain / Issue 1/2015
Electronic ISSN: 1744-8069
DOI
https://doi.org/10.1186/s12990-015-0077-3

Other articles of this Issue 1/2015

Molecular Pain 1/2015 Go to the issue