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ORIGINAL RESEARCH

Characterization of Early Inflammatory Events Leading to Provoked Vulvodynia Development in Rats

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Pages 3901-3923 | Published online: 11 Jul 2022

References

  • Bornstein J, Goldstein AT, Stockdale CK, et al. 2015 ISSVD, ISSWSH and IPPS consensus terminology and classification of persistent vulvar pain and vulvodynia. Obstet Gynecol. 2016;127(4):745–751. doi:10.1097/AOG.0000000000001359
  • Woolf CJ, Ma Q. Nociceptors—noxious stimulus detectors. Neuron. 2007;55(3):353–364. doi:10.1016/j.neuron.2007.07.016
  • Bao C, Noga H, Allaire C, et al. Provoked vestibulodynia in women with pelvic pain. Sex Med. 2019;7(2):227–234. doi:10.1016/j.esxm.2019.03.002
  • Henzell H, Berzins K, Langford JP. Provoked vestibulodynia: current perspectives. Int J Women's Health. 2017;9:631–642. doi:10.2147/IJWH.S113416
  • Akopians AL, Rapkin AJ. Vulvodynia: the role of inflammation in the etiology of localized provoked pain of the vulvar vestibule (vestibulodynia). Semin Reprod Med. 2015;33(4):239–245. doi:10.1055/s-0035-1554919
  • Lev-Sagie A, Witkin SS. Recent advances in understanding provoked vestibulodynia. F1000Research. 2016;5:2581. doi:10.12688/f1000research.9603.1
  • Aalto A, Huotari-Orava R, Luhtala S, Mäenpää J, Staff S. Expression of estrogen-related receptors in localized provoked vulvodynia. Biores Open Access. 2020;9(1):13–21. doi:10.1089/biores.2019.0049
  • Liao Z, Smith PG. Persistent genital hyperinnervation following progesterone administration to adolescent female rats. Biol Reprod. 2014;91(6):1–9. doi:10.1095/biolreprod.114.121103
  • Kalfon L, Azran A, Farajun Y, et al. Localized provoked vulvodynia: association with nerve growth factor and transient receptor potential vanilloid type 1 genes polymorphisms. J Low Genit Tract Dis. 2019;23(1):58–64. doi:10.1097/LGT.0000000000000445
  • Heddini U, Bohm-Starke N, Grönbladh A, Nyberg F, Nilsson KW, Johannesson U. Serotonin receptor gene (5HT‐2A) polymorphism is associated with provoked vestibulodynia and comorbid symptoms of pain. J Sex Med. 2014;11(12):3064–3071. doi:10.1111/jsm.12685
  • Zhang Z, Zolnoun DA, Francisco EM, Holden JK, Dennis RG, Tommerdahl M. Altered central sensitization in subgroups of women with vulvodynia. Clin J Pain. 2011;27(9):755. doi:10.1097/AJP.0b013e31821c98ec
  • Khandker M, Brady SS, Stewart EG, Harlow BL. Is chronic stress during childhood associated with adult-onset vulvodynia? J Women's Health. 2014;23(8):649–656. doi:10.1089/jwh.2013.4484
  • Witkin SS, Gerber S, Ledger WJ. Differential characterization of women with vulvar vestibulitis syndrome. Am J Obstet Gynecol. 2002;187(3):589–594. doi:10.1067/mob.2002.125889
  • Bornstein J, Palzur E. Neuroproliferative processes in vulvodynia. In: Female Sexual Pain Disorders. Wiley; 2020:43–51.
  • Farmer MA, Taylor AM, Bailey AL, et al. Repeated vulvovaginal fungal infections cause persistent pain in a mouse model of vulvodynia. Sci Transl Med. 2011;3(101):101ra91. doi:10.1126/scitranslmed.3002613
  • Gangadharan V, Kuner R. Pain hypersensitivity mechanisms at a glance. Dis Model Mech. 2013;6(4):889–895. doi:10.1242/dmm.011502
  • Honda K, Shinoda M, Kondo M, et al. Sensitization of TRPV1 and TRPA1 via peripheral mGluR5 signaling contributes to thermal and mechanical hypersensitivity. Pain. 2017;158(9):1754–1764. doi:10.1097/j.pain.0000000000000973
  • Schnegelsberg B, Sun TT, Cain G, et al. Overexpression of NGF in mouse urothelium leads to neuronal hyperinnervation, pelvic sensitivity, and changes in urinary bladder function. Am J Physiol. 2010;298(3):R534–47. doi:10.1152/ajpregu.00367.2009
  • Ji RR, Samad TA, Jin SX, Schmoll R, Woolf CJ. p38 MAPK activation by NGF in primary sensory neurons after inflammation increases TRPV1 levels and maintains heat hyperalgesia. Neuron. 2002;36(1):57–68. doi:10.1016/S0896-6273(02)00908-X
  • Obata K, Katsura H, Mizushima T, et al. TRPA1 induced in sensory neurons contributes to cold hyperalgesia after inflammation and nerve injury. J Clin Invest. 2005;115(9):2393. doi:10.1172/JCI25437
  • Zhang X, Huang J, McNaughton PA. NGF rapidly increases membrane expression of TRPV1 heat-gated ion channels. EMBO J. 2005;24(24):4211–4223. doi:10.1038/sj.emboj.7600893
  • Chadha S, Gianotten WL, Drogendijk AC, Weijmar Schultz WCM, Blindeman LAJ, van der Meijden WI. Histopathologic features of vulvar vestibulitis. Int J Gynecolog Pathol. 1998;17(1):7–11. doi:10.1097/00004347-199801000-00002
  • Regauer S, Eberz B, Beham-Schmid C. Mast cell infiltrates in vulvodynia represent secondary and idiopathic mast cell hyperplasias. APMIS. 2015;123(5):452–456. doi:10.1111/apm.12372
  • Schmelz M, Zeck S, Raithel M, Rukwied R. Mast cell tryptase in dermal neurogenic inflammation. Clin Exp Allerg. 1999;29(5):695–702. doi:10.1046/j.1365-2222.1999.00514.x
  • Leon A, Buriani A, Dal Toso R, et al. Mast cells synthesize, store, and release nerve growth factor. Proc Natl Acad Sci U S A. 1994;91(9):3739–3743. doi:10.1073/pnas.91.9.3739
  • Chatterjea D, Martinov T. Mast cells: versatile gatekeepers of pain. Mol Immunol. 2015;63(1):38. doi:10.1016/j.molimm.2014.03.001
  • Keppel Hesselink JM, Kopsky DJ, Sajben N. New topical treatment of vulvodynia based on the pathogenetic role of cross talk between nociceptors, immunocompetent cells, and epithelial cells. J Pain Res. 2016;9:757–762. doi:10.2147/JPR.S115407
  • Paavonen J, Eschenbach DA. Localized provoked vulvodynia-an ignored vulvar pain syndrome. Front Cell Infect Microbiol. 2021;11:550. doi:10.3389/fcimb.2021.678961
  • Wesselmann U, Bonham A, Foster D. Vulvodynia: current state of the biological science. Pain. 2014;155(9):1696–1701. doi:10.1016/j.pain.2014.05.010
  • Ren K, Dubner R. Interactions between the immune and nervous systems in pain. Nat Med. 2010;16(11):1267. doi:10.1038/nm.2234
  • Gupta K, Harvima IT. Mast cell-neural interactions contribute to pain and itch. Immunol Rev. 2018;282(1):168. doi:10.1111/imr.12622
  • Landry J, Martinov T, Mengistu H, et al. Repeated hapten exposure induces persistent tactile sensitivity in mice modeling localized provoked vulvodynia. Dileepan KN, ed. PLoS One. 2017;12(2):e0169672. doi:10.1371/journal.pone.0169672
  • Basha ME, Kellogg-Spadt S, Burrows LJ, et al. Thermal and mechanical pain thresholds of women with provoked localized vulvodynia: a pilot study. J Am Osteopathic Assoc. 2019;119(3):164–172. doi:10.7556/jaoa.2019.027
  • Young SH, Robinson VA, Barger M, Porter DW, Frazer DG, Castranova V. Acute inflammation and recovery in rats after intratracheal instillation of a 1→3-β-glucan (zymosan A). J Toxicol Environ Health. 2001;64(4):311–325. doi:10.1080/152873901316981303
  • Sobel JD. Vulvovaginal candidosis. Lancet. 2007;369(9577):1961–1971. doi:10.1016/S0140-6736(07)60917-9
  • da Silva EZM, Jamur MC, Oliver C. Mast cell function: a new vision of an old cell. J Histochem Cytochem. 2014;62(10):698–738. doi:10.1369/0022155414545334
  • Graham AC, Temple RM, Obar JJ. Mast cells and influenza A virus: association with allergic responses and beyond. Front Immunol. 2015;6. doi:10.3389/fimmu.2015.00238
  • Gupta S, Kakkar V, Bhushan I. Crosstalk between vaginal microbiome and female health: a review. Microb Pathog. 2019;136:103696. doi:10.1016/j.micpath.2019.103696
  • Theoharides TC, Alysandratos KD, Angelidou A, et al. Mast cells and inflammation. Biochim Biophys Acta. 2012;1822(1):21. doi:10.1016/j.bbadis.2010.12.014
  • Ben-Eli H, Solomon A. Topical antihistamines, mast cell stabilizers, and dual-action agents in ocular allergy: current trends. Current Opinion in Allergy & Clinical Immunology. 2018;18:411–416. doi:10.1097/ACI.0000000000000473
  • Anoush M, Mohammad Khani MR. Evaluating the anti-nociceptive and anti-inflammatory effects of ketotifen and fexofenadine in rats. Adv Pharm Bull. 2015;5(2):217. doi:10.15171/apb.2015.030
  • Meloto CB, Ingelmo P, Perez EV, et al. Mast cell stabilizer ketotifen fumarate reverses inflammatory but not neuropathic-induced mechanical pain in mice. Pain Rep. 2021;6(2):e902. doi:10.1097/PR9.0000000000000902
  • Sanchis-Alfonso V, Roselló -sastre E. Immunohistochemical analysis for neural markers of the lateral retinaculum in patients with isolated symptomatic patellofemoral malalignment a neuroanatomic basis for anterior knee pain in the active young patient. Am J Sports Med. 2000;28(5):725–731.
  • Bornstein J, Cohen Y, Zarfati D, Sela S, Ophir E. Involvement of heparanase in the pathogenesis of localized vulvodynia. Int J Gynecolog Pathol. 2008;27(1):136–141. doi:10.1097/pgp.0b013e318140021b
  • Tommola P, Bützow R, Unkila-Kallio L, Paavonen J, Meri S. Activation of vestibule-associated lymphoid tissue in localized provoked vulvodynia. Am J Obstet Gynecol. 2015;212(4):476.e1–476.e8. doi:10.1016/j.ajog.2014.10.1098
  • Zhu T, Zou G, Ding S, et al. Mast cell stabilizer ketotifen reduces hyperalgesia in a rodent model of surgically induced endometriosis. J Pain Res. 2019;12:1359–1369. doi:10.2147/JPR.S195909
  • Vincent L, Vang D, Nguyen J, et al. Mast cell activation contributes to sickle cell pathobiology and pain in mice. Blood. 2013;122(11):1853–1862. doi:10.1182/blood-2013-04-498105
  • Barker PA, Mantyh P, Arendt-Nielsen L, Viktrup L, Tive L. Nerve growth factor signaling and its contribution to pain. J Pain Res. 2020;13:1223–1241. doi:10.2147/JPR.S247472
  • Mai L, Liu Q, Huang F, He H, Fan W. Involvement of mast cells in the pathophysiology of pain. Front Cell Neurosci. 2021;15:205. doi:10.3389/fncel.2021.665066
  • Massaad CA, Safieh-Garabedian B, Poole S, Atweh SF, Jabbur SJ, Saadé NE. Involvement of substance P, CGRP and histamine in the hyperalgesia and cytokine upregulation induced by intraplantar injection of capsaicin in rats. J Neuroimmunol. 2004;153(1–2):171–182. doi:10.1016/j.jneuroim.2004.05.007
  • Masuoka T, Yamashita Y, Yoshida J, et al. Sensitization of glutamate receptor-mediated pain behaviour via nerve growth factor-dependent phosphorylation of transient receptor potential V1 under inflammatory conditions. Br J Pharmacol. 2020;177(18):4223–4241. doi:10.1111/bph.15176
  • Almarestani L, Longo G, Ribeiro-da-Silva A. Autonomic fiber sprouting in the skin in chronic inflammation. Mol Pain. 2008;4:1744-8069-4-56. doi:10.1186/1744-8069-4-56
  • Pitake S, Middleton LJ, Abdus-Saboor I, Mishra SK. Inflammation induced sensory nerve growth and pain hypersensitivity requires the N-type calcium channel Cav2.2. Front Neurosci. 2019;13:1009. doi:10.3389/fnins.2019.01009
  • Chung MK, Ro JY. Peripheral glutamate receptor and transient receptor potential channel mechanisms of craniofacial muscle pain. Molecular Pain. 2020;174480692091420. doi:10.1177/1744806920914204
  • Carr MJ, Undem BJ. Inflammation-induced plasticity of the afferent innervation of the airways. Environ Health Perspect. 2001;109(SUPPL. 4):567–571. doi:10.1289/ehp.01109s4567
  • Gegelashvili G, Bjerrum OJ. High-affinity glutamate transporters in chronic pain: an emerging therapeutic target. J Neurochem. 2014;131(6):712–730. doi:10.1111/jnc.12957
  • Diogenes A, Akopian AN, Hargreaves KM, El-Bialy T. NGF up-regulates TRPA1: implications for orofacial pain. The Angle Orthodontist. 2016;86(6):550–555. doi:10.1177/154405910708600612
  • Tympanidis P, Casula MA, Yiangou Y, Terenghi G, Dowd P, Anand P. Increased vanilloid receptor VR1 innervation in vulvodynia. Eur J Pain. 2004;8(2):129–133. doi:10.1016/S1090-3801(03)00085-5
  • Martinov T, Glenn-Finer R, Burley S, et al. Contact hypersensitivity to oxazolone provokes vulvar mechanical hyperalgesia in mice. PLoS One. 2013;8(10):e78673. doi:10.1371/journal.pone.0078673
  • van Diest SA, Stanisor OI, Boeckxstaens GE, de Jonge WJ, van den Wijngaard RM. Relevance of mast cell–nerve interactions in intestinal nociception. Biochimica et Biophysica Acta. 2012;1822(1):74–84. doi:10.1016/j.bbadis.2011.03.019
  • Tommola P, Unkila-Kallio L, Paetau A, Meri S, Kalso E, Paavonen J. Immune activation enhances epithelial nerve growth in provoked vestibulodynia. Am J Obstet Gynecol. 2016;215(6):768.e1–768.e8. doi:10.1016/j.ajog.2016.07.037
  • Torres-Cueco R, Nohales-Alfonso F, Luisa M, Ferrer S, Moran Sanchez I, Gonzalo JJA. Vulvodynia—it is time to accept a new understanding from a neurobiological perspective. Int J Environ Res Public Health. 2021;18(12):6639. doi:10.3390/ijerph18126639
  • Sadownik LA. Etiology, diagnosis, and clinical management of vulvodynia. Int J Women's Health. 2014;6(1):437–449. doi:10.2147/IJWH.S37660
  • Harlow BL, He W, Nguyen RHN. Allergic Reactions and Risk of Vulvodynia. Ann Epidemiol. 2009;19(11):771. doi:10.1016/j.annepidem.2009.06.006