Endometriosis-induced vaginal hyperalgesia in the rat: Role of the ectopic growths and their innervation

Pain

Volumn 147, Issue 1-3, 2009, Pages 255-264

  McAllister, Stacy L ^a   McGinty, Kristina A ^a   Resuehr, David ^a   Berkley, Karen J ^a  

^a FLORIDA STATE UNIVERSITY   (United States)

Author keywords

Estrous cycle; Gynecological pain; Neural sprouting; Sensitization; Sympathetic fibers; Vulvodynia

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CYST; DISEASE EXACERBATION; ENDOMETRIOSIS; ESTRUS; FEMALE; HYPERALGESIA; NOCICEPTION; NONHUMAN; PRIORITY JOURNAL; PROESTRUS; RAT; SYMPATHETIC INNERVATION; SYMPTOM; VAGINA DISEASE; VAGINAL HYPERALGESIA;

ANALYSIS OF VARIANCE; ANIMALS; AREA UNDER CURVE; DISEASE MODELS, ANIMAL; ENDOMETRIOSIS; ESCAPE REACTION; ESTROUS CYCLE; FEMALE; HYPERALGESIA; PAIN MEASUREMENT; PAIN THRESHOLD; PELVIC PAIN; PHYSICAL STIMULATION; RATS; TIME FACTORS; TRANSPLANTATION, AUTOLOGOUS; VAGINA;

EID: 70449642374     PISSN: 03043959     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.pain.2009.09.022     Document Type: Article

References (45)

1. Abbott J.A., Hawe J., Clayton R.D., and Garry R. The effects and effectiveness of laparoscopic excision of endometriosis: a prospective study with 2-5 year follow-up. Hum Reprod 18 (2003) 1922-1927
2. Almarestani L., Longo G., and Ribeiro-da-Silva A. Autonomic fiber sprouting in the skin in chronic inflammation. Mol Pain 4 (2008) 56
3. Anaf V., Chapron C., El Nakadi I., De Moor V., Simonart T., and Noël J.C. Pain, mast cells, and nerves in peritoneal, ovarian, and deep infiltrating endometriosis. Fertil Steril 86 (2006) 1336-1343
4. Anglin J.C., and Brooks V.L. Tyrosine hydroxylase and norepinephrine transporter in sympathetic ganglia of female rats vary with reproductive state. Auton Neurosci 105 (2003) 8-15
5. Becker J.B., Arnold A.P., Berkley K.J., Blaustein J.D., Eckel L.A., Hampson E., Herman J.P., Marts S., Sadee W., Steiner M., Taylor J., and Young E. Strategies and methods for research on sex differences in brain and behavior. Endocrinology 146 (2005) 1650-1673
6. Berkley K.J., McAllister S.L., Accius B.E., and Winnard K.P. Endometriosis-induced vaginal hyperalgesia in the rat: effect of estropause, ovariectomy, and estradiol replacement. Pain 132 (2007) S150-S159
7. Berkley K.J., Dmitrieva N., Curtis K.S., and Papka R.E. Innervation of ectopic endometrium in a rat model of endometriosis. Proc Natl Acad Sci USA 101 (2004) 11094-11098
8. Berkley K.J., Rapkin A.J., and Papka R.E. The pains of endometriosis. Science 308 (2005) 1587-1589
9. Berkley K.J., and Stratton P. Mechanisms: lessons from translational studies of endometriosis. In: Giamberardino M.A. (Ed). Visceral pain: clinical, pathophysiological and therapeutic aspects (2009), Oxford University Press, Oxford 39-49
10. Berkley K.J., Wood E., Scofield S.L., and Little M. Behavioral responses to uterine or vaginal distention in the rat. Pain 61 (1995) 121-131
11. Bradshaw H.B., and Berkley K.J. Estrogen replacement reverses ovariectomy-induced vaginal hyperalgesia in the rat. Maturitas 41 (2002) 157-165
12. Bradshaw H.B., Temple J.L., Wood E., and Berkley K.J. Estrous variations in behavioral responses to vaginal and uterine distention in the rat. Pain 82 (1999) 187-197
13. Cason A.M., Samuelsen C.L., and Berkley K.J. Estrous changes in vaginal nociception in a rat model of endometriosis. Horm Behav 44 (2003) 123-131
14. DeLeo J.A., Tanga F.Y., and Tawfik V.L. Neuroimmune activation and neuroinflammation in chronic pain and opioid tolerance/hyperalgesia. Neuroscientist 10 (2004) 40-52
15. Dmitrieva N, Nikonov A, Berkley KJ. Endometriosis (ENDO) in the rat: sensitization of afferent fibers that innervate the ectopic growths. Program No. 655.3, 2009. Neuroscience Meeting Planner. Chicago, IL: Society for Neuroscience; 2009 [online].
16. Ernsberger U. Role of neurotrophin signalling in the differentiation of neurons from dorsal root ganglia and sympathetic ganglia. Cell Tissue Res 336 (2009) 349-384
17. Freeman M.E. The neuroendocrine control of the ovarian cycle of the rat. In: Neill J.D. (Ed). Knobil and Neill's physiology of reproduction. 3rd ed. (2006), Academic Press, San Diego 2327-2388
18. Gibbs G.F., Drummond P.D., Finch P.M., and Phillips J.K. Unravelling the pathophysiology of complex regional pain syndrome: focus on sympathetically maintained pain. Clin Exp Pharmacol Physiol 35 (2008) 717-724
19. Giudice L.C., and Kao L.C. Endometriosis. Lancet 364 (2004) 1789-1799
20. Gonzalez M.I., Field M.J., Bramwell S., McCleary S., and Singh L. Ovariohysterectomy in the rat: a model of surgical pain for evaluation of pre-emptive analgesia?. Pain 88 (2000) 79-88
21. Jänig W., Levine J.D., and Michaelis M. Interactions of sympathetic and primary afferent neurons following nerve injury and tissue trauma. Prog Brain Res 113 (1996) 161-184
22. Jesch N.K., Kuebler J.F., Nguyen H., Nave H., Bottlaender M., Teichmann B., Braun A., Vieten G., and Ure B.M. Laparoscopy vs minilaparotomy and full laparotomy preserves circulatory but not peritoneal and pulmonary immune responses. J Pediatr Surg 41 (2006) 1085-1092
23. Ji R.R., and Woolf C.J. Neuronal plasticity and signal transduction in nociceptive neurons: implications for the initiation and maintenance of pathological pain. Neurobiol Dis 8 (2001) 1-10
24. Kaur G., Janik J., Isaacson L.G., and Callahan P. Estrogen regulation of neurotrophin expression in sympathetic neurons and vascular targets. Brain Res 1139 (2007) 6-14
25. Khasar S.G., Green P.G., and Levine J.D. Repeated sound stress enhances inflammatory pain in the rat. Pain 116 (2005) 79-86
26. Lee T.M., Lin M.S., and Chang N.C. Physiological concentration of 17beta-estradiol on sympathetic reinnervation in ovariectomized infarcted rats. Endocrinology 149 (2008) 1205-1213
27. Lu K.H., Hopper B.R., Vargo T.M., and Yen S.S. Chronological changes in sex steroid, gonadotropin and prolactin secretions in aging female rats displaying different reproductive states. Biol Reprod 21 (1979) 193-203
28. McMahon S.B. NGF as a mediator of inflammatory pain. Philos Trans R Soc Lond B Biol Sci 351 (1996) 431-440
29. McMahon S.B., Cafferty W.B., and Marchand F. Immune and glial cell factors as pain mediators and modulators. Exp Neurol 192 (2005) 444-462
30. Melzack R., Coderre T.J., Katz J., and Vaccarino A.L. Central neuroplasticity and pathological pain. Ann N Y Acad Sci 933 (2001) 157-174
31. Mendell L.M., Albers K.M., and Davis B.M. Neurotrophins, nociceptors, and pain. Microsc Res Tech 45 (1999) 252-261
32. Morán C., Franco A., Morán J.L., Handal A., Morales L., and Domínguez R. Neural activity between ovaries and the prevertebral celiac-superior mesenteric ganglia varies during the estrous cycle of the rat. Endocrine 26 (2005) 147-152
33. Morrison T.C., Dmitrieva N., Winnard K.P., and Berkley K.J. Opposing viscerovisceral effects of surgically induced endometriosis and a control abdominal surgery on the rat bladder. Fertil Steril 86 (2006) 1067-1073
34. Nagabukuro H., and Berkley K.J. Influence of endometriosis on visceromotor and cardiovascular responses induced by vaginal distention in the rat. Pain 132 (2007) S96-S103
35. Papka R.E., McNeill D.L., Thompson D., and Schmidt H.H. Nitric oxide nerves in the uterus are parasympathetic, sensory, and contain neuropeptides. Cell Tissue Res 279 (1995) 339-349
36. Ren K., and Dubner R. Neuron-glia crosstalk gets serious: role in pain hypersensitivity. Curr Opin Anaesthesiol 21 (2008) 570-579
37. Shakiba K., Bena J.F., McGill K.M., Minger J., and Falcone T. Surgical treatment of endometriosis: a 7-year follow-up on the requirement for further surgery. Obstet Gynecol 111 (2008) 1285-1292
38. Sharpe-Timms K.L. Using rats as a research model for the study of endometriosis. Ann N Y Acad Sci 955 (2002) 318-327
39. Somigliana E., Vigano P., Barbara G., and Vercellini P. Treatment of endometriosis-related pain: options and outcomes. Front Biosci (Elite Ed) 1 (2009) 455-465
40. Ting A.Y., Blacklock A.D., and Smith P.G. Estrogen regulates vaginal sensory and autonomic nerve density in the rat. Biol Reprod 71 (2004) 1397-1404
41. Vercellini P., Fedele L., Aimi G., Pietropaolo G., Consonni D., and Crosignani P.G. Association between endometriosis stage, lesion type, patient characteristics and severity of pelvic pain symptoms: a multivariate analysis of over 1000 patients. Hum Reprod 22 (2007) 266-271
42. Vernon M.W., and Wilson E.A. Studies on the surgical induction of endometriosis in the rat. Fertil Steril 44 (1985) 684-694
43. Wallace V.C., Blackbeard J., Segerdahl A.R., Hasnie F., Pheby T., McMahon S.B., and Rice A.S. Characterization of rodent models of HIV-gp120 and anti-retroviral-associated neuropathic pain. Brain 130 (2007) 2688-2702
44. Weihe E., Schafer M.K., Erickson J.D., and Eiden L.E. Localization of vesicular monoamine transporter isoforms (VMAT1 and VMAT2) to endocrine cells and neurons in rat. J Mol Neurosci 5 (1994) 149-164
45. Zhang G., Dmitrieva N., Liu Y., McGinty K.A., and Berkley K.J. Endometriosis as a neurovascular condition: estrous variations in innervation, vascularization, and growth factor content of ectopic endometrial cysts in the rat. Am J Physiol Regul Integr Comp Physiol 294 (2008) R162-R171