Neonatal morphine enhances nociception and decreases analgesia in young rats

Brain Research

Volumn 1199, Issue , 2008, Pages 82-90

  Zhang, Guo Hua ^a   Sweitzer, Sarah M ^a  

^a UNIVERSITY OF SOUTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

Allodynia; Hyperalgesia; Morphine; Neonatal rat; Stress induced analgesia

Indexed keywords

MORPHINE; OPIATE DERIVATIVE; SODIUM CHLORIDE;

ANALGESIA; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; DRUG DOSE INCREASE; FEMALE; INTENSIVE CARE UNIT; LONG TERM EXPOSURE; MALE; NEWBORN; NOCICEPTION; NONHUMAN; PERINATAL PERIOD; PRENATAL PERIOD; PRIORITY JOURNAL; RAT; STRESS; SWIMMING; THIRD TRIMESTER PREGNANCY;

RATTUS;

EID: 40049093900     PISSN: 00068993     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.brainres.2007.12.043     Document Type: Article

References (74)

1. Abbadie C. Lombard M.C. Besson J.M. Trafton J.A. Basbaum A.I. Mu and delta opioid receptor-like immunoreactivity in the cervical spinal cord of the rat after dorsal rhizotomy or neonatal capsaicin: an analysis of pre- and postsynaptic receptor distributions Brain Res. 930 2002 150 162
2. Al-Chaer E.D. Kawasaki M. Pasricha P.J. A new model of chronic visceral hypersensitivity in adult rats induced by colon irritation during postnatal development Gastroenterology 119 2000 1276 1285
3. Alvares D. Torsney C. Beland B. Reynolds M. Fitzgerald M. Modelling the prolonged effects of neonatal pain Prog. Brain Res. 129 2000 365 373
4. Anand K.J. Coskun V. Thrivikraman K.V. Nemeroff C.B. Plotsky P.M. Long-term behavioral effects of repetitive pain in neonatal rat pups Physiol. Behav. 66 1999 627 637
5. Andrews K. Fitzgerald M. The cutaneous withdrawal reflex in human neonates: sensitization, receptive fields, and the effects of contralateral stimulation Pain 56 1994 95 101
6. Angst M.S. Clark J.D. Opioid-induced hyperalgesia: a qualitative systematic review Anesthesiology 104 2006 570 587
7. Angst M.S. Koppert W. Pahl I. Clark D.J. Schmelz M. Short-term infusion of the mu-opioid agonist remifentanil in humans causes hyperalgesia during withdrawal Pain 106 2003 49 57
8. Arnold J.H. Truog R.D. Orav E.J. Scavone J.M. Hershenson M.B. Tolerance and dependence in neonates sedated with fentanyl during extracorporeal membrane oxygenation Anesthesiology 73 1990 1136 1140
9. Barron S. Riley E.P. Pup-induced maternal behavior in adult and juvenile rats exposed to alcohol prenatally Alcohol Clin. Exp. Res. 9 1985 360 365
10. Bederson J.B. Fields H.L. Barbaro N.M. Hyperalgesia during naloxone-precipitated withdrawal from morphine is associated with increased on-cell activity in the rostral ventromedial medulla Somatosens. Motor Res. 7 1990 185 203
11. Beland B. Fitzgerald M. Mu- and delta-opioid receptors are downregulated in the largest diameter primary sensory neurons during postnatal development in rats Pain 90 2001 143 150
12. Besse D. Lombard M.C. Zajac J.M. Roques B.P. Besson J.M. Pre- and postsynaptic distribution of mu, delta and kappa opioid receptors in the superficial layers of the cervical dorsal horn of the rat spinal cord Brain Res. 521 1990 15 22
13. Boucher T. Jennings E. Fitzgerald M. The onset of diffuse noxious inhibitory controls in postnatal rat pups: a C-Fos study Neurosci. Lett. 257 1998 9 12
14. Carbajal R. Lenclen R. Jugie M. Paupe A. Barton B.A. Anand K.J. Morphine does not provide adequate analgesia for acute procedural pain among preterm neonates Pediatrics 115 2005 1494 1500
15. Celerier E. Rivat C. Jun Y. Laulin J.P. Larcher A. Reynier P. Simonnet G. Long-lasting hyperalgesia induced by fentanyl in rats: preventive effect of ketamine Anesthesiology 92 2000 465 472
16. Champagne F. Meaney M.J. Like mother, like daughter: evidence for non-genomic transmission of parental behavior and stress responsivity Prog. Brain Res. 133 2001 287 302
17. Champagne F.A. Francis D.D. Mar A. Meaney M.J. Variations in maternal care in the rat as a mediating influence for the effects of environment on development Physiol. Behav. 79 2003 359 371
18. Chu L.F. Clark D.J. Angst M.S. Opioid tolerance and hyperalgesia in chronic pain patients after one month of oral morphine therapy: a preliminary prospective study J. Pain 7 2006 43 48
19. Compton M.A. Cold-pressor pain tolerance in opiate and cocaine abusers: correlates of drug type and use status J. Pain Symptom Manage 9 1994 462 473
20. Compton P. Charuvastra V.C. Kintaudi K. Ling W. Pain responses in methadone-maintained opioid abusers J. Pain Symptom Manage 20 2000 237 245
21. Compton P. Charuvastra V.C. Ling W. Pain intolerance in opioid-maintained former opiate addicts: effect of long-acting maintenance agent Drug Alcohol Depend. 63 2001 139 146
22. Craig K.D. Whitfield M.F. Grunau R.V. Linton J. Hadjistavropoulos H.D. Pain in the preterm neonate: behavioural and physiological indices Pain 52 1993 287 299
23. Dickenson A. Rahman W. Mechanisms of chronic pain and the developing nervous system P. McGrath Chronic and Recurrent Pain in Children and Adolescents vol. 13 1999 IASP Press Seattle 5 38
24. Dickenson A.H. Sullivan A.F. Knox R. Zajac J.M. Roques B.P. Opioid receptor subtypes in the rat spinal cord: electrophysiological studies with mu- and delta-opioid receptor agonists in the control of nociception Brain Res. 413 1987 36 44
25. Djouhri L. Lawson S.N. Abeta-fiber nociceptive primary afferent neurons: a review of incidence and properties in relation to other afferent A-fiber neurons in mammals Brain Res. Brain Res. Rev. 46 2004 131 145
26. Dobbing J. Later development of the brain and its vulnerability J.A. Davis J. Dobbing Scientific Foundations of Paediatrics vol. 2 1981 William Heinemann London 744 759
27. Doverty M. Somogyi A.A. White J.M. Bochner F. Beare C.H. Menelaou A. Ling W. Methadone maintenance patients are cross-tolerant to the antinociceptive effects of morphine Pain 93 2001 155 163
28. Doverty M. White J.M. Somogyi A.A. Bochner F. Ali R. Ling W. Hyperalgesic responses in methadone maintenance patients Pain 90 2001 91 96
29. Faber E.S. Chambers J.P. Brugger F. Evans R.H. Depression of A and C fibre-evoked segmental reflexes by morphine and clonidine in the in vitro spinal cord of the neonatal rat Br. J. Pharmacol. 120 1997 1390 1396
30. Fitzgerald M. Jennings E. The postnatal development of spinal sensory processing Proc. Natl. Acad. Sci. U. S. A. 96 1999 7719 7722
31. Fitzgerald M. Koltzenburg M. The functional development of descending inhibitory pathways in the dorsolateral funiculus of the newborn rat spinal cord Brain Res. 389 1986 261 270
32. Fitzgerald M. Shaw A. MacIntosh N. Postnatal development of the cutaneous flexor reflex: comparative study of preterm infants and newborn rat pups Dev. Med. Child Neurol. 30 1988 520 526
33. Fitzgerald M. Millard C. McIntosh N. Cutaneous hypersensitivity following peripheral tissue damage in newborn infants and its reversal with topical anaesthesia Pain 39 1989 31 36
34. Fitzgerald M. Butcher T. Shortland P. Developmental changes in the laminar termination of A fibre cutaneous sensory afferents in the rat spinal cord dorsal horn J. Comp. Neurol. 348 1994 225 233
35. Fleming A.S. O'Day D.H. Kraemer G.W. Neurobiology of mother-infant interactions: experience and central nervous system plasticity across development and generations Neurosci. Biobehav. Rev. 23 1999 673 685
36. Franck L. Vilardi J. Assessment and management of opioid withdrawal in ill neonates Neonatal Netw. 14 1995 39 48
37. Franck L.S. Vilardi J. Durand D. Powers R. Opioid withdrawal in neonates after continuous infusions of morphine or fentanyl during extracorporeal membrane oxygenation Am. J. Crit. Care 7 1998 364 369
38. French J.P. Nocera M. Drug withdrawal symptoms in children after continuous infusions of fentanyl J. Pediatr. Nurs. 9 1994 107 113
39. Gilbert M. Stelzner D.J. The development of descending and dorsal root connections in the lumbosacral spinal cord of the postnatal rat J. Comp. Neurol. 184 1979 821 838
40. Gonzalez D. Fuchs J. Droge M. Neurosci. Lett. 151 1993 134 137
41. Grunau R.V. Whitfield M.F. Petrie J.H. Fryer E.L. Early pain experience, child and family factors, as precursors of somatization: a prospective study of extremely premature and fullterm children Pain 56 1994 353 359
42. Grunau R.E. Holsti L. Peters J.W. Long-term consequences of pain in human neonates Semin. Fetal Neonatal Med. 11 2006 268 275
43. Ho A. Dole V.P. Pain perception in drug-free and in methadone-maintained human ex-addicts Proc. Soc. Exp. Biol. Med. 162 1979 392 395
44. Hori Y. Kanda K. Dev. Brain Res. 80 1994 141 148
45. Huot R.L. Thrivikraman K.V. Meaney M.J. Plotsky P.M. Development of adult ethanol preference and anxiety as a consequence of neonatal maternal separation in Long Evans rats and reversal with antidepressant treatment Psychopharmacology (Berl) 158 2001 366 373
46. Johnston C.C. Stevens B.J. Yang F. Horton L. Differential response to pain by very premature neonates Pain 61 1995 471 479
47. Johnston C.C. Stevens B. Yang F. Horton L. Developmental changes in response to heelstick in preterm infants: a prospective cohort study Dev. Med. Child Neurol. 38 1996 438 445
48. Jones T. Sweitzer S. Wilson S. Yeomans D. Afferent fiber selective shift in opiate potency following targeted opioid receptor knockdown Pain 106 2003 365 371
49. Kim D.H. Fields H.L. Barbaro N.M. Morphine analgesia and acute physical dependence: rapid onset of two opposing, dose-related processes Brain Res. 516 1990 37 40
50. Leong S.K. Shieh J.Y. Wong W.C. Localizing spinal-cord-projecting neurons in neonatal and immature albino rats J. Comp. Neurol. 228 1984 18 23
51. Lidow M.S. Long-term effects of neonatal pain on nociceptive systems Pain 99 2002 377 383
52. Lidow M. Song Z. Ren K. Long-term effects of short-lasting early local inflammatory insult Neuroreport 12 2001 399 403
53. Lin C. Al-Chaer E.D. Long-term sensitization of primary afferents in adult rats exposed to neonatal colon pain Brain Res. 971 2003 73 82
54. Lu Y. Pirec V. Yeomans D.C. Differential antinociceptive effects of spinal opioids on foot withdrawal responses evoked by C fibre or A delta nociceptor activation Br. J. Pharmacol. 121 1997 1210 1216
55. Malanga C.J. Kosofsky B.E. Does drug abuse beget drug abuse? Behavioral analysis of addiction liability in animal models of prenatal drug exposure Brain Res. Dev. Brain Res. 147 2003 47 57
56. Mao J. Opioid-induced abnormal pain sensitivity: implications in clinical opioid therapy Pain 100 2002 213 217
57. Meaney M.J. Maternal care, gene expression, and the transmission of individual differences in stress reactivity across generations Annu. Rev. Neurosci. 24 2001 1161 1192
58. Mogil J.S. Sternberg W.F. Balian H. Liebeskind J.C. Sadowski B. Opioid and nonopioid swim stress-induced analgesia: a parametric analysis in mice Physiol. Behav. 59 1996 123 132
59. Nandi R. Beacham D. Middleton J. Koltzenburg M. Howard R.F. Fitzgerald M. The functional expression of mu opioid receptors on sensory neurons is developmentally regulated; morphine analgesia is less selective in the neonate Pain 111 2004 38 50
60. Norton S.J. Aftereffects of morphine and fentanyl analgesia: a retrospective study Neonatal Netw. 7 1988 25 28
61. Oberlander T.F. Grunau R.E. Whitfield M.F. Fitzgerald C. Pitfield S. Saul J.P. Biobehavioral pain responses in former extremely low birth weight infants at four months' corrected age Pediatrics 105 2000 e6
62. Peng Y.B. Ling Q.D. Ruda M.A. Kenshalo D.R. Electrophysiological changes in adult rat dorsal horn neurons after neonatal peripheral inflammation J. Neurophysiol. 90 2003 73 80
63. Peters J.W. Schouw R. Anand K.J. van Dijk M. Duivenvoorden H.J. Tibboel D. Does neonatal surgery lead to increased pain sensitivity in later childhood? Pain 114 2005 444 454
64. Rahman W. Dickenson A.H. Development of spinal opioid systems Reg. Anesth. Pain Med. 24 1999 383 385
65. Rahman W. Dashwood M.R. Fitzgerald M. Aynsley-Green A. Dickenson A.H. Postnatal development of multiple opioid receptors in the spinal cord and development of spinal morphine analgesia Brain Res. Dev. Brain Res. 108 1998 239 254
66. Ruda M.A. Ling Q.D. Hohmann A.G. Peng Y.B. Tachibana T. Altered nociceptive neuronal circuits after neonatal peripheral inflammation Science 289 2000 628 631
67. Saigal S. Feeny D. Furlong W. Rosenbaum P. Burrows E. Torrance G. Comparison of the health-related quality of life of extremely low birth weight children and a reference group of children at age eight years J. Pediatr. 125 1994 418 425
68. Simons S.H. van Dijk M. van Lingen R.A. Roofthooft D. Duivenvoorden H.J. Jongeneel N. Bunkers C. Smink E. Anand K.J. van den Anker J.N. Tibboel D. Routine morphine infusion in preterm newborns who received ventilatory support: a randomized controlled trial Jama 290 2003 2419 2427
69. Sweitzer S. Wong S. Tjolsen A. Allen C. Mochly-Rosen D. Kendig J.J. Exaggerated nociceptive responses on morphine withdrawal: roles of protein kinase C epsilon and gamma Pain 110 2004 281 289
70. Sweitzer S.M. Allen C.P. Zissen M.H. Kendig J.J. Mechanical allodynia and thermal hyperalgesia upon acute opioid withdrawal in the neonatal rat Pain 110 2004 269 280
71. Taddio A. Katz J. The effects of early pain experience in neonates on pain responses in infancy and childhood Paediatr. Drugs 7 2005 245 257
72. Taddio A. Stevens B. Craig K. Rastogi P. Ben-David S. Shennan A. Mulligan P. Koren G. Efficacy and safety of lidocaine–prilocaine cream for pain during circumcision N. Engl. J. Med. 336 1997 1197 1201
73. Zissen M.H. Zhang G. Kendig J.J. Sweitzer S.M. Acute and chronic morphine alters formalin pain in neonatal rats Neurosci. Lett. 400 2006 154 157
74. Zissen M.H. Zhang G. McKelvy A. Propst J.T. Kendig J.J. Sweitzer S.M. Tolerance, opioid-induced allodynia and withdrawal associated allodynia in infant and young rats Neuroscience 144 2007 247 262