Neonatal Cystitis Makes Adult Female Rat Urinary Bladders More Sensitive to Low Concentration Microbial Antigens

References

• Clemens JQ, Mullins C, Ackerman AL, et al. Urologic chronic pelvic pain syndrome: insights from the MAPP Research Network. Nat Rev Urol. 2019;16(3):187–200. doi:10.1038/s41585-018-0135-5
   PubMed Web of Science ®Google Scholar
• Birder L. Pathophysiology of interstitial cystitis. Inter J Urol. 2019;2019(S1):12–15. doi:10.1111/iju.13985
   Google Scholar
• Rahnama’i MS, Javan A, Vyas N, et al. Bladder pain syndrome and interstitial cystitis beyond horizon: reports from the Global Interstitial Cystitis/Bladder Pain Society (GIBS) meeting 2019 Mumbai-India. Anesth Pain Med. 2020;10:e101848.
   PubMedGoogle Scholar
• Khullar V, Chermansky C, Tarcan T, et al. How can we improve the diagnosis and management of bladder pain syndrome? Part 1: ICI-RS 2018. Neurourol Neurodyn. 2019;38:S66–S70.
   PubMedGoogle Scholar
• Sutcliffe S, Bradley CS, Clemens JQ, et al. Urologic chronic pelvic pain syndrome flares and their impact: qualitative analysis in the MAPP Network. Int Urogynecol J. 2015;26(7):1047–1060. doi:10.1007/s00192-015-2652-6
   PubMed Web of Science ®Google Scholar
• Sutcliffe S, Jemielita T, Lai HH, et al. A case-crossover study of urologic chronic pelvic pain syndrome flare triggers in the MAPP Research Network. J Urol. 2018;199(5):1245–1251. doi:10.1016/j.juro.2017.12.050
   PubMed Web of Science ®Google Scholar
• Warren JW. Interstitial cystitis as an infectious disease. Urol Clin North Am. 1994;21(1):3–39. doi:10.1016/S0094-0143(21)00589-9
   Web of Science ®Google Scholar
• Warren JW, Brown V, Jacobs S, Horne L, Langenberg P, Greenberg P. Urinary tract infection and inflammation at onset of interstitial cystitis/painful bladder syndrome. Urol. 2008;71(6):1085–1090. doi:10.1016/j.urology.2007.12.091
   PubMed Web of Science ®Google Scholar
• Wilson ML, Gaido L. Laboratory diagnosis of urinary tract infections in adult patients. Med Micro. 2004;38:1150–1158.
   Google Scholar
• Chu CM, Lowder JL. Diagnosis and treatment of urinary tract infections across age groups. Am J Obstet Gynecol. 2018;219(1):40–51. doi:10.1016/j.ajog.2017.12.231
   PubMed Web of Science ®Google Scholar
• Kupelian AS, Horsley H, Khasiriya R, et al. Discrediting microscopic pyuria and leucocyte esterase as diagnostic surrogates for infection in patients with lower urinary tract symptoms: results from a clinical and laboratory evaluation. BJU Int. 2013;112(2):231–238. doi:10.1111/j.1464-410X.2012.11694.x
   PubMed Web of Science ®Google Scholar
• Stanford E, McMurphy C. There is a low incidence of recurrent bacteriuria in painful bladder syndrome/interstitial cystitis patients followed longitudinally. Int Urogynecol J Pelvic Floor Dysfunct. 2007;18(5):551–554. doi:10.1007/s00192-006-0184-9
   PubMed Web of Science ®Google Scholar
• Nickel JC, Stephens A, Landis JR, et al. Urinary fungi associated with urinary symptom severity among women with interstitial cystitis/bladder pain syndrome (IC/BPS). World J Urol. 2020;38(2):433–446. doi:10.1007/s00345-019-02764-0
   PubMed Web of Science ®Google Scholar
• Nickel JC, Stephens A, Landis JR, et al. Assessment of the lower urinary tract microbiota during symptom flare in women with urologic chronic pelvic pain syndrome: a MAPP Network Study. J Urol. 2016;195(2):356–362. doi:10.1016/j.juro.2015.09.075
   PubMed Web of Science ®Google Scholar
• Nickel JC, Stephens A, Landis JR, et al. A culture-independent analysis of the microbiota of female interstitial cystitis/bladder pain syndrome participants in the MAPP Research Network. J Clin Med. 2019;8(3):415. doi:10.3390/jcm8030415
   PubMed Web of Science ®Google Scholar
• Peters KM, Killinger KA, Ibrahim IA. Childhood symptoms and events in women with interstitial cystitis/painful bladder syndrome. Urology. 2009;73(2):258–262. doi:10.1016/j.urology.2008.09.014
   PubMed Web of Science ®Google Scholar
• Ness T, DeWitte C, DeBerry J, et al. A model in female rats with phenotypic features similar to interstitial cystitis/bladder pain syndrome. Front Pain Res. 2021;7:791045. doi:10.3389/fpain.2021.791045
   Google Scholar
• Randich A, Uzzell TW, DeBerry JJ, Ness TJ. Neonatal urinary bladder inflammation produces adult bladder hypersensitivity. J Pain. 2006;7(7):469–479. doi:10.1016/j.jpain.2006.01.450
   PubMed Web of Science ®Google Scholar
• Schwaller F, Fitzgerald M. The consequences of pain in early life: injury-induced plasticity in developing pain pathways. Eur J Neurosci. 2014;39(3):344–352. doi:10.1111/ejn.12414
   PubMed Web of Science ®Google Scholar
• DeBerry J, Randich A, Shaffer A, Robbins M, Ness TJ. Neonatal bladder inflammation produces functional changes and alters neuropeptide content in bladders of adult female rats. J Pain. 2010;11(3):247–255. doi:10.1016/j.jpain.2009.07.010
   PubMed Web of Science ®Google Scholar
• Ness TJ, Randich A. Neonatal bladder inflammation alters activity of adult rat spinal visceral nociceptive neurons. Neurosci Lett. 2010;472(3):210–214. doi:10.1016/j.neulet.2010.02.007
   PubMed Web of Science ®Google Scholar
• Saban MR, Hellmich H, Nguyen N-B, et al. Time-course of LPS-induced gene expression in a mouse model of genitourinary inflammation. Physiol Genomics. 2001;5(3):147–160. doi:10.1152/physiolgenomics.2001.5.3.147
   PubMed Web of Science ®Google Scholar
• Randich A, Uzzell TW, Cannon RS, Ness TJ. Inflammation and enhanced nociceptive responses to bladder distension produced by intravesical zymosan in the rat. BMC Urol. 2006;6(1):2. doi:10.1186/1471-2490-6-2
   PubMedGoogle Scholar
• Castroman P, Ness TJ. Vigor of visceromotor responses to urinary bladder distension in rats increases with repeated trials and stimulus intensity. Neurosci Letts. 2001;306(1–2):97–100. doi:10.1016/S0304-3940(01)01886-9
   PubMed Web of Science ®Google Scholar
• Kogan P, Xu S, Wang Y, et al. Subnoxious intravesical lipopolysaccharide triggers bladder inflammation and symptom onset in a transgenic autoimmune cystitis model: a MAPP Network Animal Study. Sci Rep. 2018;8(1):6573. doi:10.1038/s41598-018-24833-x
   PubMedGoogle Scholar
• Cui X, Jing X, Lutgendorf SK, et al. Cystitis-induced bladder pain is Toll-like receptor 4 dependent in a transgenic autoimmune cystitis murine model: a MAPP Research Network animal study. Am J Physiol. 2019;317:F90–F98.
   Google Scholar
• Moghadam SO, Zowroozi MR. Toll-like receptors: the role in bladder cancer development, progression and immunotherapy. Scan J Immunol. 2019;90(6):e12818. doi:10.1111/sji.12818
   PubMed Web of Science ®Google Scholar
• Niemczyk G, Fus L, Czarzasta K, et al. Expression of Toll-like receptors in the animal model of bladder outlet obstruction. Biomed Res Int. 2020;2020:6632359. doi:10.1155/2020/6632359
   PubMed Web of Science ®Google Scholar
• Samuelsson P, Hang L, Wullt B, Irjala H, Svanborg C. Toll-like receptor 4 expression and cytokine responses in the human urinary tract mucosa. Infect Immun. 2004;72(6):3179–3186. doi:10.1128/IAI.72.6.3179-3186.2004
   PubMed Web of Science ®Google Scholar
• Montalbetti N, Dalghi MG, Bastacky SI, et al. Bladder infection with uropathogenic E. Coli increases the excitability of afferent neurons. Am J Physiol. 2022;322:F1–F13.
   Google Scholar
• Parsons CL. The potassium sensitivity test: a new gold standard for diagnosing and understanding the pathophysiology of interstitial cystitis. J Urol. 2009;182(2):432–434. doi:10.1016/j.juro.2009.04.089
   PubMed Web of Science ®Google Scholar
• Ness TJ, DeWitte C, Randich A. Neonatal cystitis leads to alterations in spinal corticotropin releasing factor receptor-type 2 content and function in adult rats following bladder re-inflammation. Brain Res. 2022;1788:147927. doi:10.1016/j.brainres.2022.147927
   PubMed Web of Science ®Google Scholar
• Shaffer AD, Ness TJ, Robbins MT, Randich A. Early in life bladder inflammation alters opioid peptide content in the spinal cord and bladder of adult female rats. J Urol. 2013;189(1):352–358. doi:10.1016/j.juro.2012.08.190
   PubMed Web of Science ®Google Scholar
• Tabansky I, Moldwin RM, Liu M, et al. A shared B-cell clonotype inpatients with Interstitial Cystitis/Bladder Pain Syndrome presenting with Hunner lesions. Continence Rep. 2022;4:100015. doi:10.1016/j.contre.2022.100015
   Google Scholar
• Yoshizumi M, Tazawa N, Watanabe C, Mizoguchi H. TRPV4 activation prevents lipopolysaccharide-induced painful bladder hypersensitivity in rats by regulating immune pathways. Front Immunol. 2022;2022:1080302. doi:10.3389/fimmu.2022.1080302
   Google Scholar
• Wang X, Fan L, Yin H, et al. Protective effect of Aster tataricus extract on NLRP3-mediated pyroptosis of bladder urothelial cells. J Cell Mol Med. 2020;24(22):13336–13345. doi:10.1111/jcmm.15952
   PubMed Web of Science ®Google Scholar
• Podmolikova L, Mukanyangezi MF, Dahlqvist AJ, Naluai AT, Ny L, Giglio D. Radiation of the urinary bladder attenuates the development of lipopolysaccharide-induced cystitis. Int Immunopharmacol. 2020;83:106334. doi:10.1016/j.intimp.2020.106334
   PubMed Web of Science ®Google Scholar
• Lee KW, Kim WB, Lee SW, et al. Alterations of macrophage migration inhibitory factor expression in the nervous system of the rat cystitis model. Urol Int. 2017;98(2):228–235. doi:10.1159/000456077
   PubMed Web of Science ®Google Scholar
• Korgali E, Dundar G, Coskun KA, et al. Effect of strontium chloride on experimental bladder inflammation in rat. Int Scholar Res Not. 2014;2014:369292.
   PubMedGoogle Scholar
• Lecci A, Birder LA, Meini S, et al. Pharmacological evaluation of the role of cyclooxygenase isoenzymes on the micturition reflex following experimental cystitis in rats. Br J Phamacol. 2000;130(2):331–338. doi:10.1038/sj.bjp.0703309
   PubMed Web of Science ®Google Scholar
• Luber-Narod J, Austin-Ritchie T, Hollins C, et al. Role of substance P in several models of bladder inflammation. Urol Res. 1997;25(6):395–399. doi:10.1007/BF01268854
   PubMedGoogle Scholar
• Shin JH, Ryu C-M, Ju H, et al. Synergistic effects of N-acetylcysteine and mesenchymal stem cell in a lipopolysaccharide-induced interstitial cystitis rat model. Cells. 2020;9(1):86. doi:10.3390/cells9010086
   Web of Science ®Google Scholar
• Ryu C-M, Shin JH, Yu HY, et al. N-acetylcysteine prevents bladder tissue fibrosis in a lipopolysaccharide-induced cystitis rat model. Sci Reps. 2019;9(1):8134. doi:10.1038/s41598-019-44631-3
   PubMedGoogle Scholar
• Li J, Luo H, Dong X, et al. Therapeutic effect of urine-derived stem cells for protamine/lipopolysaccharide-induced interstitial cystitis in a rat model. Stem Cell Res Ther. 2017;8(1):107. doi:10.1186/s13287-017-0547-9
   PubMedGoogle Scholar
• Choi B-H, Jin L-H, Kim K-H, et al. Mast cell activation and response to tolterodine in the rat urinary bladder in a chronic model of intravesical protamine sulfate and bacterial endotoxin-induced cystitis. Mol Med Rep. 2014;10(2):670–676. doi:10.3892/mmr.2014.2262
   PubMed Web of Science ®Google Scholar
• Sinanoglu O, Ekici ID, Ekici S. Comparison of intravesical application of chondroitin sulfate and colchicine in rat protamine/lipopolysaccharide induced cystitis model. Urol J. 2014;11(1):1296–1300.
   PubMed Web of Science ®Google Scholar
• Lv J, Huang Y, Zhu S, et al. MCP-1-induced histamine release from mast cells is associated with development of interstitial cystitis/bladder pain syndrome in rat models. Mediators Inflamm. 2012;2012:358184. doi:10.1155/2012/358184
   PubMed Web of Science ®Google Scholar
• Shao Y, Lu G-L, Shen Z-J, He H-C. Reduction of intercellular adhesion molecule 1 may play a role in anti-inflammatory effect of hyaluronic acid in a rat model of severe non-bacterial cystitis. World J Urol. 2013;31(3):535–540. doi:10.1007/s00345-012-0839-8
   PubMed Web of Science ®Google Scholar
• Stein PC, Pham H, Ito T, Parsons CL. Bladder injury model induced in rats by exposure to protamine sulfate followed by bacterial endotoxin. J Urol. 1996;155(3):1133–1138. doi:10.1016/S0022-5347(01)66406-1
   PubMed Web of Science ®Google Scholar
• Meyer-Siegler KL, Ordorica RC, Vera PL. Macrophage migration inhibitory factor is upregulated in an endotoxin-induced model of bladder inflammation in rats. J Interferon Cytokine Res. 2004;24(1):55–63. doi:10.1089/107999004772719918
   PubMed Web of Science ®Google Scholar
• Lecci A, Tramontana M, Giuliani S, Criscuoli M, Maggi CA. Effect of Tachykinin NK 2 receptor blockade on detrusor hyperreflexia induced by bacterial toxin in RATS. J Urol. 1998;160(1):206–209. doi:10.1016/S0022-5347(01)63091-X
   PubMed Web of Science ®Google Scholar
• Diaz-Salmeron R, Cailleau C, Denis S, Ponchel G, Bouchemal K. Hyaluronan nanoplatelets exert an intrinsic anti-inflammatory activity in a rat model of bladder painful syndrome/interstitial cystitis. J Control Release. 2023;356:434–447. doi:10.1016/j.jconrel.2023.03.014
   PubMed Web of Science ®Google Scholar
• Rosen JM, Klumpp DJ. Mechanisms of pain from urinary tract infection. Int J Urol. 2014;21(S1):26–32. doi:10.1111/iju.12309
   PubMedGoogle Scholar
• Horvath DJ, Patel AS, Mohamed A, et al. Association of O-antigen serotype with the magnitude of initial systemic cytokine responses and persistence in the urinary tract. J Bacteriol. 2016;198(6):964–972. doi:10.1128/JB.00664-15
   PubMed Web of Science ®Google Scholar
• Ball CL, Ness TJ, Randich A. Opioid blockade and inflammation reveal estrous cycle effects on visceromotor reflexes evoked by bladder distension. J Urol. 2010;184(4):1529–1535. doi:10.1016/j.juro.2010.05.090
   PubMed Web of Science ®Google Scholar
• Arshad M, Seed PC. Urinary tract infections in the infant. Clin Perinatol. 2015;42(1):17–28. doi:10.1016/j.clp.2014.10.003
   PubMed Web of Science ®Google Scholar
• Harb A, Yassine V, Ghssein G, Salami A, Fakih H. Prevalence and clinical significance of urinary tract infection among neonates presenting with unexplained hyperbilirubinemia inLebanaon: a retrospective study. Infect Chemother. 2023;55(2):194–203. doi:10.3947/ic.2022.0117
   PubMed Web of Science ®Google Scholar
• Swamy S, Barcella W, De Iorio M, et al. Recalcitrant chronic bladder pain and recurrent cystitis but negative urinalysis: what should we do? Int Urogyn J. 2018;29(7):1035–1043. doi:10.1007/s00192-018-3569-7
   PubMed Web of Science ®Google Scholar
• Swamy S, Kupelian AS, Khasriya RR, et al. Cross-over data supporting long-term antibiotic treatment in patients with painful lower urinary tract symptoms, pyuria and negative urinalysis. Int Urogynecol J. 2019;30(3):409–414. doi:10.1007/s00192-018-3846-5
   PubMed Web of Science ®Google Scholar
• Kawasaki T, Kawai T. Toll-like receptor signaling pathways. Front Immunol. 2014;5:461. doi:10.3389/fimmu.2014.00461
   PubMed Web of Science ®Google Scholar
• Oliveira-Nascimento L, Massari P, Wetzler LM. The role of TLR2 in infection and immunity. Front Immunol. 2012;3:79. doi:10.3389/fimmu.2012.00079
   PubMed Web of Science ®Google Scholar