The Journal of Pain
Volume 11, Issue 3 , Pages 247-255 , March 2010

Neonatal Bladder Inflammation Produces Functional Changes and Alters Neuropeptide Content in Bladders of Adult Female Rats

  • Jennifer DeBerry

      Affiliations

    • Department of Psychology, University of Alabama at Birmingham
  • ,
  • Alan Randich

      Affiliations

    • Department of Psychology, University of Alabama at Birmingham
  • ,
  • Amber D. Shaffer

      Affiliations

    • Department of Psychology, University of Alabama at Birmingham
  • ,
  • Meredith T. Robbins

      Affiliations

    • Department of Anesthesiology, University of Alabama at Birmingham
  • ,
  • Timothy J. Ness

      Affiliations

    • Department of Anesthesiology, University of Alabama at Birmingham
    • Corresponding Author InformationAddress reprint requests to Dr Timothy J. Ness, Department of Anesthesiology, 901 19th Street South, BMR2-Room 270, Birmingham, AL 35205.

Received 14 April 2009 ,Revised 28 May 2009 ,Accepted 22 July 2009.

References 

  1. Al-Chaer ED, Kawasaki M, Pasricha PJ. A new model of chronic visceral hypersensitivity in adult rats induced by colon irritation during postnatal development. Gastroenterol. 2000;119:1276–1285
  2. Blatt LK, Lashinger ES, Laping NJ, Su X. Evaluation of pressor and visceromotor reflex responses to bladder distension in urethane anesthetized rats. Neurourol Urodyn. 2009;28:442–446
  3. Blom JM, Benatti C, Alboni S, Capone G, Ferraguti C, Brunello N, et al. Early postnatal chronic inflammation produces long-term changes in pain behaviour and N-methyl-D-aspartate receptor subtype gene expression in the central nervous system of adult mice. J Neurosci Res. 2006;84:1789–1798
  4. Chertin B, Rolle U, Cascio S, Puri P. Alterations in cholinergic and neuropeptide innervation of urinary bladder following partial bladder outlet obstruction. Pediatr Surg Int. 2003;19:427–431
  5. Chitkara DK, van Tilburg MA, Blois-Martin N, Whitehead WE. Early life risk factors that contribute to irritable bowel syndrome in adults: A systematic review. Am J Gastroenterol. 2008;103:765–774
  6. Chu Y-C, Chan K-H, Tsou M-Y, Lin S-M, Hsieh Y-C, Tao Y-X. 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;106:1204–1212
  7. Christmas TJ, Rode J, Chapple CR, Milroy EJ, Turner-Warwick RT. Nerve fibre proliferation in interstitial cystitis. Virchows Arch A Pathol Anat Histopathol. 1990;416:447–451
  8. DeBerry J, Ness TJ, Robbins MT, Randich A. Inflammation-induced enhancement of the visceromotor reflex to urinary bladder distension: Modulation by endogenous opioids and the effects of early-in-life experience with bladder inflammation. J Pain. 2007;8:914–923
  9. Fitzgerald M. The development of nociceptive circuits. Nat Rev Neurosci. 2005;6:507–520
  10. Geppetti P, Nassini R, Materazzi S, Benemei S. The concept of neurogenic inflammation. BJU Int. 2008;101(Suppl 3):2–6
  11. Hathway G, Harrop E, Baccei M, Walker S, Moss A, Fitzgerald M. A postnatal switch in GABAergic control of spinal cutaneous reflexes. Eur J Neurosci. 2006;23:112–118
  12. Hargreaves K, Dubner R, Brown R, Flores C, Joris J. A new and sensitive method for measuring thermal nociception in cutaneous hyperalgesia. Pain. 1988;32:77–88
  13. Hermann C, Hohmeister J, Demirakca S, Zohsel K, Flor H. Long-term alteration of pain sensitivity in school-aged children and early pain experiences. Pain. 2006;125:278–285
  14. Hohmann AG, Neely MH, Pina J, Nackley AG. Neonatal chronic hind paw inflammation alters sensitization to intradermal capsaicin in adult rats: A behavioral and immunocytochemical study. J Pain. 2005;6:798–808
  15. Howell S, Poulton R, Talley NJ. The natural history of childhood abdominal pain and its association with adult irritable bowel syndrome: Birth-cohort study. Am J Gastroenterol. 2005;100:2071–2078
  16. Jaggar SI, Scott HC, Rice ASC. Inflammation of the rat urinary bladder is associated with a referred thermal hyperalgesia which is nerve growth factor dependent. Br J Anaesth. 1999;83:442–448
  17. Johnson OL, Berkley KJ. Estrous influences on micturition thresholds of the female rat before and after bladder inflammation. Am J Physiol Regul Integr Comp Physiol. 2002;282:R289–R294
  18. Jones CA, Nyberg L. Epidemiology of interstitial cystitis. Urology. 1997;49(Suppl 5A):2–9
  19. Koltzenburg M, McMahon SB. Plasma extravasation in the rat urinary bladder following mechanical, electrical and chemical stimuli: Evidence for a new population of chemosensitive primary sensory afferents. Neurosci Lett. 1986;72:352–356
  20. Lamb K, Gebhart GF, Bielefeldt K. Increased nerve growth factor expression triggers bladder overactivity. J Pain. 2004;5:150–156
  21. LaPrairie JL, Murphy AZ. Female rats are more vulnerable to the long-term consequences of neonatal inflammatory injury. Pain. 2007;132(Suppl 1):S124–S133
  22. LaPrairie JL, Johns ME, Murphy AZ. Preemptive morphine analgesia attenuates the long-term consequences of neonatal inflammation in male and female rats. Pediatr Res. 2008;64:625–630
  23. Li J, Baccei ML. Excitatory synapses in the rat superficial dorsal horn are strengthened following peripheral inflammation during early postnatal development. Pain. 2009;143:56–64
  24. Lidow MS, Song ZM, Ren K. Long-term effects of short-lasting early local inflammatory insult. Neuroreport. 2001;12:399–403
  25. Lin C, Al-Chaer ED. Long-term sensitization of primary afferents in adult rats exposed to neonatal colon pain. Brain Res. 2003;971:73–82
  26. Liu LS, Winston JH, Shenoy MM, Song GQ, Chen JD, Pasricha PJ. A rat model of chronic gastric sensorimotor dysfunction resulting from transient neonatal gastric irritation. Gastroenterol. 2008;134:2070–2079
  27. Long JA, Evans HM. The estrous cycle in the rat and its associated phenomena. Mem Univ Calif. 1922;6:1–148
  28. Mallen CD, Peat G, Thomas E, Croft PR. Is chronic pain in adulthood related to childhood factors? A population-based case-control study of young adults. J Rheumatol. 2006;33:2286–2290
  29. Michaelis M, Habler HJ, Jaenig W. Silent afferents: A separate class of primary afferents?. Clin Exp Pharmacol Physiol. 1996;23:99–105
  30. Ness TJ, Lewis-Sides A, Castroman P. Characterization of pressor and visceromotor reflex responses to bladder distension in rats: Sources of variability and effect of analgesics. J Urol. 2001;165:968–974
  31. Peeker R, Enerback L, Fall M, Aldenborg F. Recruitment, distribution and phenotypes of mast cells in interstitial cystitis. J Urol. 2000;163:1009–1015
  32. Peng YB, Ling QD, Ruda MA, Kenshalo DR. Electrophysiological changes in adult rat dorsal horn neurons after neonatal peripheral inflammation. J Neurophysiol. 2003;90:73–80
  33. Randich A, Mebane H, Ness TJ. Ice water testing reveals hypersensitivity in adult rats that experienced neonatal bladder inflammation: Implications for painful bladder syndrome/interstitial cystitis. J Urol. 2009;182:337–342
  34. Randich A, Uzzell T, Cannon R, Ness TJ. Inflammation and enhanced nociceptive responses to bladder distension produced by intravesical zymosan in the rat. BMC Urol. 2006;6:2
  35. Randich A, Uzzell T, DeBerry JJ, Ness TJ. Neonatal urinary bladder inflammation produces adult bladder hypersensitivity. J Pain. 2006;7:469–479
  36. Ren K, Anseloni V, Zou S-P, Wade EB, Novikova SI, Ennis M, et al. Characterization of basal and re-inflammation associated long-term alteration in pain responsivity following short-lasting neonatal local inflammatory insult. Pain. 2004;110:588–596
  37. Ren K, Novikova SI, He F, Dubner R, Lidow MS. Neonatal local noxious insult affects gene expression in the spinal dorsal horn of adult rats. Mol Pain. 2005;1:27
  38. Rice ASC. Topical spinal administration of a nitric oxide synthase inhibitor prevents the hyper-reflexia associated with a rat model of persistent visceral pain. Neurosci Lett. 1995;187:111–114
  39. Ruda MA, Ling Q-D, Hohmann AG, Peng YB, Tachibana T. Altered nociceptive neuronal circuits after neonatal peripheral inflammation. Science. 2000;289:628–631
  40. Saab CY, Wang J, Gu C, Garner KN, Al-Chaer ED. Microglia: A newly discovered role in visceral hypersensitivity?. Neuron Glia Biol. 2007;2:271–277
  41. Sant GR, Kempuraj D, Marchand JE, Theoharides TC. The mast cell in interstitial cystitis: Role in pathophysiology and pathogenesis. Urology. 2007;69(Suppl 4):34–40
  42. Smith C, Nordstrom E, Sengupta JN, Miranda A. Neonatal gastric suctioning results in chronic visceral and somatic hyperalgesia: Role of corticotropin releasing factor. Neurogastroenterol Motil. 2007;19:692–699
  43. Smith PP, Hurtado E, Smith CP, Boone TB, Somogyi GT. Comparison of cystometric methods in female rats. Neurourol Urodyn. 2008;27:324–329
  44. Tachibana T, Ling Q-D, Ruda MA. Increased Fos induction in adult rats that experienced neonatal peripheral inflammation. Neuroreport. 2001;12:925–927
  45. Taddio A, Katz J. The effects of early pain experience in neonates on pain responses in infancy and childhood. Paediatr Drugs. 2005;7:245–257
  46. Tian S-L, Wang X-Y, Ding G-H. Repeated electro-acupuncture attenuates chronic visceral hypersensitivity and spinal cord NMDA receptor phosphorylation in a rat irritable bowel syndrome model. Life Sci. 2008;83:356–363
  47. Walker SM. Pain in children: Recent advances and ongoing challenges. Br J Anaesth. 2008;101:101–110
  48. Walker SM, Franck LS, Fitzgerald M, Myles J, Stocks J, Marlow N. Long-term impact of neonatal intensive care and surgery on somatosensory perception in children born extremely preterm. Pain. 2009;141:79–87
  49. Wang J, Gu C, Al-Chaer E. Altered behavior and digestive outcomes in adult male rats primed with minimal colon pain as neonates. Behav Brain Funct. 2008;4:28
  50. Winston J, Shenoy M, Medley D, Naniwadekar A, Pasricha PJ. The vanilloid receptor initiates and maintains colonic hypersensitivity induced by neonatal colon irritation in rats. Gastroenterol. 2007;132:615–627
  51. Wollgarten-Hadamek I, Hohmeister J, Demirakca S, Zohsel K, Flor H, Hermann C. Do burn injuries during infancy affect pain and sensory sensitivity in later childhood?. Pain. 2009;141:165–172
  52. Woolf CJ, Salter MW. Neuronal plasticity: Increasing the gain in pain. Science. 2000;288:1765–1769
  53. Xu G-Y, Shenoy M, Winston JH, Mittal S, Pasricha PJ. P2X receptor-mediated visceral hyperalgesia in a rat model of chronic visceral hypersensitivity. Gut. 2008;57:1230–1237

 Supported by National Institutes of Health grants DK51413, DK073218 and DK078655.

PII: S1526-5900(09)00657-9

doi: 10.1016/j.jpain.2009.07.010

The Journal of Pain
Volume 11, Issue 3 , Pages 247-255 , March 2010