Best Practice & Research Clinical Gastroenterology
Volume 22, Issue 1 , Pages 31-44 , February 2008

Pancreatic pain

  • Helmut Friess, MD (Professor and Chairman)

      Affiliations

    • Corresponding Author InformationCorresponding author. Tel.: +49 89 4140 2121; Fax: +49 89 4140 4870.

References 

  1. Sarles H, Bernard JP, Johnson C. Pathogenesis and epidemiology of chronic pancreatitis. Annu Rev Med. 1989;40:453–468
  2. Adler G, Schmid RM. Chronic pancreatitis: still puzzling?. Gastroenterology. 1997;112:1762–1765
  3. Dimagno EP. A short, eclectic history of exocrine pancreatic insufficiency and chronic pancreatitis. Gastroenterology. 1993;104:1255–1262
  4. Malfertheiner P, Buchler M, Stanescu A, et al. Exocrine pancreatic function in correlation to ductal and parenchymal morphology in chronic pancreatitis. Hepatogastroenterology. 1986;33:110–114
  5. Sarner M, Cotton PB. Definitions of acute and chronic pancreatitis. Clin Gastroenterol. 1984;13:865–870
  6. Ammann RW, Muellhaupt B. The natural history of pain in alcoholic chronic pancreatitis. Gastroenterology. 1999;116:1132–1140
  7. Gullo L, Barbara L. Treatment of pancreatic pseudocysts with octreotide. Lancet. 1991;338:540–541
  8. Ebbehoj N, Borly L, Bulow J, et al. Pancreatic tissue fluid pressure in chronic pancreatitis. Relation to pain, morphology, and function. Scand J Gastroenterol. 1990;25:1046–1051
  9. Ebbehoj N. Pancreatic tissue fluid pressure and pain in chronic pancreatitis. Dan Med Bull. 1992;39:128–133
  10. Bradley EL. Pancreatic duct pressure in chronic pancreatitis. Am J Surg. 1982;144:313–316
  11. Di Sebastiano P, di Mola FF, Buchler MW, et al. Pathogenesis of pain in chronic pancreatitis. Dig Dis. 2004;22:267–272
  12. Di Sebastiano P, Fink T, Weihe E, et al. Immune cell infiltration and growth-associated protein 43 expression correlate with pain in chronic pancreatitis. Gastroenterology. 1997;112:1648–1655
  13. Freelove R, Walling AD. Pancreatic cancer: diagnosis and management. Am Fam Physician. 2006;73:485–492
  14. Greenwald HP, Bonica JJ, Bergner M. The prevalence of pain in four cancers. Cancer. 1987;60:2563–2569
  15. Krech RL, Walsh D. Symptoms of pancreatic cancer. J Pain Symptom Manage. 1991;6:360–367
  16. Caraceni A, Portenoy RK. Pain management in patients with pancreatic carcinoma. Cancer. 1996;78:639–653
  17. Bockman DE. Cells of origin of pancreatic cancer: experimental animal tumors related to human pancreas. Cancer. 1981;47:1528–1534
  18. Bockman DE, Buchler M, Malfertheiner P, et al. Analysis of nerves in chronic pancreatitis. Gastroenterology. 1988;94:1459–1469
  19. Keith RG, Keshavjee SH, Kerenyi NR. Neuropathology of chronic pancreatitis in humans. Can J Surg. 1985;28:207–211
  20. Di Sebastiano P, di Mola FF, Bockman DE, et al. Chronic pancreatitis: the perspective of pain generation by neuroimmune interaction. Gut. 2003;52:907–911
  21. Liddle RA, Nathan JD. Neurogenic inflammation and pancreatitis. Pancreatology. 2004;4(6):551–559discussion 559--560. Epub 2004 Nov 15
  22. Di Sebastiano P, Fink T, di Mola FF, et al. Neuroimmune appendicitis. Lancet. 1999;354:461–466
  23. Weihe E, Nohr D, Muller S, et al. The tachykinin neuroimmune connection in inflammatory pain. Ann N Y Acad Sci. 1991;632:283–295
  24. Duggan AW, Hendry IA, Morton CR, et al. Cutaneous stimuli releasing immunoreactive substance P in the dorsal horn of the cat. Brain Res. 1988;451:261–273
  25. Di Sebastiano P, di Mola FF, Di Febbo C, et al. Expression of interleukin 8 (IL-8) and substance P in human chronic pancreatitis. Gut. 2000;47:423–428
  26. Santoni G, Perfumi MC, Pompei P, et al. Impairment of rat thymocyte differentiation and functions by neonatal capsaicin treatment is associated with induction of apoptosis. J Neuroimmunol. 2000;104:37–46
  27. Joos GF, Pauwels RA. Pro-inflammatory effects of substance P: new perspectives for the treatment of airway diseases?. Trends Pharmacol Sci. 2000;21:131–133
  28. Bhatia M, Brady M, Shokuhi S, et al. Inflammatory mediators in acute pancreatitis. J Pathol. 2000;190:117–125
  29. Buchler M, Weihe E, Friess H, et al. Changes in peptidergic innervation in chronic pancreatitis. Pancreas. 1992;7:183–192
  30. Shrikhande SV, Friess H, di Mola FF, et al. NK-1 receptor gene expression is related to pain in chronic pancreatitis. Pain. 2001;91:209–217
  31. McMahon SB. NGF as a mediator of inflammatory pain. Philos Trans R Soc Lond B Biol Sci. 1996;351:431–440
  32. Aloe L, Tuveri MA, Levi-Montalcini R. Studies on carrageenan-induced arthritis in adult rats: presence of nerve growth factor and role of sympathetic innervation. Rheumatol Int. 1992;12:213–216
  33. Brown MC, Perry VH, Lunn ER, et al. Macrophage dependence of peripheral sensory nerve regeneration: possible involvement of nerve growth factor. Neuron. 1991;6:359–370
  34. Leon A, Buriani A, Dal TR, et al. Mast cells synthesize, store, and release nerve growth factor. Proc Natl Acad Sci USA. 1994;91:3739–3743
  35. Heumann R, Korsching S, Bandtlow C, et al. Changes of nerve growth factor synthesis in nonneuronal cells in response to sciatic nerve transection. J Cell Biol. 1987;104:1623–1631
  36. Matsuoka I, Meyer M, Thoenen H. Cell-type-specific regulation of nerve growth factor (NGF) synthesis in non-neuronal cells: comparison of Schwann cells with other cell types. J Neurosci. 1991;11:3165–3177
  37. Friess H, Zhu ZW, di Mola FF, et al. Nerve growth factor and its high-affinity receptor in chronic pancreatitis. Ann Surg. 1999;230:615–624
  38. Andreev N, Urban L, Dray A. Opioids suppress spontaneous activity of polymodal nociceptors in rat paw skin induced by ultraviolet irradiation. Neuroscience. 1994;58:793–798
  39. Petty BG, Cornblath DR, Adornato BT, et al. The effect of systemically administered recombinant human nerve growth factor in healthy human subjects. Ann Neurol. 1994;36:244–246
  40. Donnerer J, Schuligoi R, Stein C. Increased content and transport of substance P and calcitonin gene-related peptide in sensory nerves innervating inflamed tissue: evidence for a regulatory function of nerve growth factor in vivo. Neuroscience. 1992;49:693–698
  41. Leslie TA, Emson PC, Dowd PM, et al. Nerve growth factor contributes to the up-regulation of growth-associated protein 43 and preprotachykinin A messenger RNAs in primary sensory neurons following peripheral inflammation. Neuroscience. 1995;67:753–761
  42. Lindsay RM, Harmar AJ. Nerve growth factor regulates expression of neuropeptide genes in adult sensory neurons. Nature. 1989;337:362–364
  43. Lindsay RM, Lockett C, Sternberg J, et al. Neuropeptide expression in cultures of adult sensory neurons: modulation of substance P and calcitonin gene-related peptide levels by nerve growth factor. Neuroscience. 1989;33:53–65
  44. Friess H, Shrikhande S, Shrikhande M, et al. Neural alterations in surgical stage chronic pancreatitis are independent of the underlying aetiology. Gut. 2002;50:682–686
  45. Fink T, Di Sebastiano P, Buchler M, et al. Growth-associated protein-43 and protein gene-product 9.5 innervation in human pancreas: changes in chronic pancreatitis. Neuroscience. 1994;63:249–266
  46. Zhu ZW, Friess H, Wang L, et al. Brain-derived neurotrophic factor (BDNF) is upregulated and associated with pain in chronic pancreatitis. Dig Dis Sci. 2001;46:1633–1639
  47. Ceyhan GO, Bergmann F, Kadihasanoglu M, et al. The neurotrophic factor artemin influences the extent of neural damage and growth in chronic pancreatitis. Gut. 2007;56:534–544
  48. Bolon B, Jing S, Asuncion F, et al. The candidate neuroprotective agent artemin induces autonomic neural dysplasia without preventing peripheral nerve dysfunction. Toxicol Pathol. 2004;32:275–294
  49. Elitt CM, McIlwrath SL, Lawson JJ, et al. Artemin overexpression in skin enhances expression of TRPV1 and TRPA1 in cutaneous sensory neurons and leads to behavioral sensitivity to heat and cold. J Neurosci. 2006;26:8578–8587
  50. Malin SA, Molliver DC, Koerber HR, et al. Glial cell line-derived neurotrophic factor family members sensitize nociceptors in vitro and produce thermal hyperalgesia in vivo. J Neurosci. 2006;26:8588–8599
  51. Orozco OE, Walus L, Sah DW, et al. GFRalpha3 is expressed predominantly in nociceptive sensory neurons. Eur J Neurosci. 2001;13:2177–2182
  52. Sofroniew MV, Howe CL, Mobley WC. Nerve growth factor signaling, neuroprotection, and neural repair. Annu Rev Neurosci. 2001;24:1217–1281
  53. Chao MV. Neurotrophins and their receptors: a convergence point for many signalling pathways. Nat Rev Neurosci. 2003;4:299–309
  54. Paveliev M, Airaksinen MS, Saarma M. GDNF family ligands activate multiple events during axonal growth in mature sensory neurons. Mol Cell Neurosci. 2004;25:453–459
  55. Yan H, Newgreen DF, Young HM. Developmental changes in neurite outgrowth responses of dorsal root and sympathetic ganglia to GDNF, neurturin, and artemin. Dev Dyn. 2003;227:395–401
  56. Curtis R, Green D, Lindsay RM, et al. Up-regulation of GAP-43 and growth of axons in rat spinal cord after compression injury. J Neurocytol. 1993;22:51–64
  57. Curtis R. Growth-associated protein-43 (GAP-43) is expressed by glial cells of the central and peripheral nervous system. Ann N Y Acad Sci. 1993;679:407–411
  58. Skene JH. Axonal growth-associated proteins. Annu Rev Neurosci. 1989;12:127–156
  59. Nakao A, Harada A, Nonami T, et al. Clinical significance of carcinoma invasion of the extrapancreatic nerve plexus in pancreatic cancer. Pancreas. 1996;12:357–361
  60. Takahashi T, Ishikura H, Motohara T, et al. Perineural invasion by ductal adenocarcinoma of the pancreas. J Surg Oncol. 1997;65:164–170
  61. Okusaka T, Okada S, Ueno H, et al. Abdominal pain in patients with resectable pancreatic cancer with reference to clinicopathologic findings. Pancreas. 2001;22:279–284
  62. Liu B, Lu KY. Neural invasion in pancreatic carcinoma. Hepatobiliary Pancreat Dis Int. 2002;1:469–476
  63. Hirai I, Kimura W, Ozawa K, et al. Perineural invasion in pancreatic cancer. Pancreas. 2002;24:15–25
  64. Pour PM, Egami H, Takiyama Y. Patterns of growth and metastases of induced pancreatic cancer in relation to the prognosis and its clinical implications. Gastroenterology. 1991;100:529–536
  65. Bockman DE, Buchler M, Beger HG. Interaction of pancreatic ductal carcinoma with nerves leads to nerve damage. Gastroenterology. 1994;107:219–230
  66. Zhu Z, Friess H, diMola FF, et al. Nerve growth factor expression correlates with perineural invasion and pain in human pancreatic cancer. J Clin Oncol. 1999;17:2419–2428
  67. Zhu Z, Kleeff J, Kayed H, et al. Nerve growth factor and enhancement of proliferation, invasion, and tumorigenicity of pancreatic cancer cells. Mol Carcinog. 2002;35:138–147
  68. Miknyoczki SJ, Lang D, Huang L, et al. Neurotrophins and Trk receptors in human pancreatic ductal adenocarcinoma: expression patterns and effects on in vitro invasive behavior. Int J Cancer. 1999;81:417–427
  69. Ketterer K, Rao S, Friess H, et al. Reverse transcription-PCR analysis of laser-captured cells points to potential paracrine and autocrine actions of neurotrophins in pancreatic cancer. Clin Cancer Res. 2003;9:5127–5136
  70. Funahashi H, Takeyama H, Sawai H, et al. Alteration of integrin expression by glial cell line-derived neurotrophic factor (GDNF) in human pancreatic cancer cells. Pancreas. 2003;27:190–196
  71. Funahashi H, Okada Y, Sawai H, et al. The role of glial cell line-derived neurotrophic factor (GDNF) and integrins for invasion and metastasis in human pancreatic cancer cells. J Surg Oncol. 2005;91:77–83
  72. Ceyhan GO, Giese NA, Erkan M, et al. The neurotrophic factor artemin promotes pancreatic cancer invasion. Ann Surg. 2006;244:274–281
  73. Friess H, Zhu Z, Liard V, et al. Neurokinin-1 receptor expression and its potential effects on tumor growth in human pancreatic cancer. Lab Invest. 2003;83:731–742
  74. Liddle RA. The role of Transient Receptor Potential Vanilloid 1 (TRPV1) channels in pancreatitis. Biochim Biophys Acta. 2007 Aug;1772(8):869–878Epub 2007 Mar 1
  75. Michael GJ, Priestley JV. Differential expression of the mRNA for the vanilloid receptor subtype 1 in cells of the adult rat dorsal root and nodose ganglia and its downregulation by axotomy. J Neurosci. 1999;19:1844–1854
  76. Immke DC, Gavva NR. The TRPV1 receptor and nociception. Semin Cell Dev Biol. 2006;17:582–591
  77. Michalski CW, Laukert T, Sauliunaite D, et al. Cannabinoids ameliorate pain and reduce disease pathology in cerulein-induced acute pancreatitis. Gastroenterology. 2007;132:1968–1978
  78. Van Der Stelt M, Di Marzo, Endovanilloids V. Putative endogenous ligands of transient receptor potential vanilloid 1 channels. Eur J Biochem. 2004;271:1827–1834
  79. Nicol GD, Lopshire JC, Pafford CM. Tumor necrosis factor enhances the capsaicin sensitivity of rat sensory neurons. J Neurosci. 1997;17:975–982
  80. Hartel M, di Mola FF, Selvaggi F, et al. Vanilloids in pancreatic cancer: potential for chemotherapy and pain management. Gut. 2006;55:519–528
  81. Nathan JD, Patel AA, McVey DC, et al. Capsaicin vanilloid receptor-1 mediates substance P release in experimental pancreatitis. Am J Physiol Gastrointest Liver Physiol. 2001;281:G1322–G1328
  82. Nathan JD, Peng RY, Wang Y, et al. Primary sensory neurons: a common final pathway for inflammation in experimental pancreatitis in rats. Am J Physiol Gastrointest Liver Physiol. 2002;283:G938–G946
  83. Hutter MM, Wick EC, Day AL, et al. Transient receptor potential vanilloid (TRPV-1) promotes neurogenic inflammation in the pancreas via activation of the neurokinin-1 receptor (NK-1R). Pancreas. 2005;30:260–265
  84. Wick EC, Hoge SG, Grahn SW, et al. Transient receptor potential vanilloid 1, calcitonin gene-related peptide, and substance P mediate nociception in acute pancreatitis. Am J Physiol Gastrointest Liver Physiol. 2006;290:G959–G969
  85. Xu GY, Winston JH, Shenoy M, et al. Transient receptor potential vanilloid 1 mediates hyperalgesia and is up-regulated in rats with chronic pancreatitis. Gastroenterology. 2007 Oct;133(4):1282–1292Epub 2007 Jun 20
  86. Shu X, Mendell LM. Nerve growth factor acutely sensitizes the response of adult rat sensory neurons to capsaicin. Neurosci Lett. 1999;274:159–162
  87. Dimcevski G, Sami SA, Funch-Jensen P, et al. Pain in chronic pancreatitis: the role of reorganization in the central nervous system. Gastroenterology. 2007;132:1546–1556
  88. Michalski CW, Shi X, Reiser C, et al. Neurokinin-2 receptor levels correlate with intensity, frequency and duration of pain in chronic pancreatitis. Ann Surg. 2007 Nov;246(5):786–793
  89. Drapiewski JR. Carcinoma of the pancreas: A study of neoplastic invasion of nerves and its possible clinical significance. Am J Clin Pathol. 1944;14:549–555

PII: S1521-6918(07)00122-9

doi: 10.1016/j.bpg.2007.10.016

Best Practice & Research Clinical Gastroenterology
Volume 22, Issue 1 , Pages 31-44 , February 2008