Abstract
Purpose
Low amplitude rhythmic contractions (LARC) occur in detrusor smooth muscle and may play a role in storage disorders such as overactive bladder and detrusor overactivity. The purpose of this study was to determine whether LARC frequencies identified in vitro from strips of human urinary bladder tissue correlate with in vivo LARC frequencies, visualized as phasic intravesical pressure (p ves) waves during urodynamics (UD).
Methods
After IRB approval, fresh strips of human urinary bladder were obtained from patients. LARC was recorded with tissue strips at low tension (<2 g) and analyzed by fast Fourier transform (FFT) to identify LARC signal frequencies. Blinded UD tracings were retrospectively reviewed for signs of LARC on the p ves tracing during filling and were analyzed via FFT.
Results
Distinct LARC frequencies were identified in 100% of tissue strips (n = 9) obtained with a mean frequency of 1.97 ± 0.47 cycles/min (33 ± 8 mHz). Out of 100 consecutive UD studies reviewed, 35 visually displayed phasic p ves waves. In 12/35 (34%), real p ves signals were present that were independent of abdominal activity. Average UD LARC frequency was 2.34 ± 0.36 cycles/min (39 ± 6 mHz) which was similar to tissue LARC frequencies (p = 0.50). A majority (83%) of the UD cohort with LARC signals also demonstrated detrusor overactivity.
Conclusions
During UD, a subset of patients displayed phasic p ves waves with a distinct rhythmic frequency similar to the in vitro LARC frequency quantified in human urinary bladder tissue strips. Further refinements of this technique may help identify subsets of individuals with LARC—mediated storage disorders.
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References
Brading AF (2006) Spontaneous activity of lower urinary tract smooth muscles: correlation between ion channels and tissue function. J Physiol 570(Pt 1):13–22. doi:10.1113/jphysiol.2005.097311
Byrne MD, Klausner AP, Speich JE, Southern JB, Habibi JR, Ratz PH (2013) Fourier transform analysis of rabbit detrusor autonomous contractions reveals length dependent increases in tone and slow wave development at long lengths. J Urol 190(1):334–340. doi:10.1016/j.juro.2013.02.071
Drake MJ, Harvey IJ, Gillespie JI, Van Duyl WA (2005) Localized contractions in the normal human bladder and in urinary urgency. BJU Int 95(7):1002–1005. doi:10.1111/j.1464-410X.2005.05455.x
Hashitani H, Brading AF (2003) Ionic basis for the regulation of spontaneous excitation in detrusor smooth muscle cells of the guinea-pig urinary bladder. Br J Pharmacol 140(1):159–169. doi:10.1038/sj.bjp.0705320
Andersson KE (2010) Detrusor myocyte activity and afferent signaling. Neurourol Urodyn 29(1):97–106. doi:10.1002/nau.20784
Almasri AM, Ratz PH, Bhatia H, Klausner AP, Speich JE (2010) Rhythmic contraction generates adjustable passive stiffness in rabbit detrusor. J Appl Physiol 108(3):544–553. doi:10.1152/japplphysiol.01079.2009
Birder L, Andersson KE (2013) Urothelial signaling. Physiol Rev 93(2):653–680. doi:10.1152/physrev.00030.2012
McCloskey KD (2013) Bladder interstitial cells: an updated review of current knowledge. Acta Physiol 207(1):7–15. doi:10.1111/apha.12009
Hashitani H, Lang RJ (2010) Functions of ICC-like cells in the urinary tract and male genital organs. J Cell Mol Med 14(6A):1199–1211. doi:10.1111/j.1582-4934.2010.01043.x
Gray SM, McGeown JG, McMurray G, McCloskey KD (2013) Functional innervation of Guinea-pig bladder interstitial cells of cajal subtypes: neurogenic stimulation evokes in situ calcium transients. PLoS One 8(1):e53423. doi:10.1371/journal.pone.0053423
Sui G, Fry CH, Malone-Lee J, Wu C (2009) Aberrant Ca2+ oscillations in smooth muscle cells from overactive human bladders. Cell Calcium 45(5):456–464. doi:10.1016/j.ceca.2009.03.001
Kinder RB, Mundy AR (1987) Pathophysiology of idiopathic detrusor instability and detrusor hyper-reflexia. An in vitro study of human detrusor muscle. Br J Urol 60(6):509–515
Smith PP, DeAngelis A, Simon R (2015) Evidence of increased centrally enhanced bladder compliance with ageing in a mouse model. BJU Int 115(2):322–329. doi:10.1111/bju.12669
Lentle RG, Reynolds GW, Janssen PW, Hulls CM, King QM, Chambers JP (2015) Characterisation of the contractile dynamics of the resting ex vivo urinary bladder of the pig. BJU Int 116(6):973–983. doi:10.1111/bju.13132
Szell EA, Somogyi GT, de Groat WC, Szigeti GP (2003) Developmental changes in spontaneous smooth muscle activity in the neonatal rat urinary bladder. Am J Physiol Regul Integr Comp Physiol 285(4):R809–R816. doi:10.1152/ajpregu.00641.2002
Potjer RM, Constantinou CE (1989) Frequency of spontaneous contractions in longitudinal and transverse bladder strips. Am J Physiol 257(4 Pt 2):R781–R787
Sibley GN (1984) A comparison of spontaneous and nerve-mediated activity in bladder muscle from man, pig and rabbit. J Physiol 354:431–443
Buckner SA, Milicic I, Daza AV, Coghlan MJ, Gopalakrishnan M (2002) Spontaneous phasic activity of the pig urinary bladder smooth muscle: characteristics and sensitivity to potassium channel modulators. Br J Pharmacol 135(3):639–648. doi:10.1038/sj.bjp.0704499
Winters JC, Dmochowski RR, Goldman HB, Herndon CD, Kobashi KC, Kraus SR, Lemack GE, Nitti VW, Rovner ES, Wein AJ, American Urological A, Society of Urodynamics FPM, Urogenital R (2012) Urodynamic studies in adults: AUA/SUFU guideline. J Urol 188(6 Suppl):2464–2472. doi:10.1016/j.juro.2012.09.081
Colhoun AF, Klausner AP, Nagle AS, Carroll AW, Barbee RW, Ratz PH, Speich JE (2016) A pilot study to measure dynamic elasticity of the bladder during urodynamics. Neurourol Urodyn. doi:10.1002/nau.23043
Speich JE, Wilson CW, Almasri AM, Southern JB, Klausner AP, Ratz PH (2012) Carbachol-induced volume adaptation in mouse bladder and length adaptation via rhythmic contraction in rabbit detrusor. Ann Biomed Eng 40(10):2266–2276. doi:10.1007/s10439-012-0590-8
Colhoun AF, Speich JE, Dolat MT, Habibi JR, Guruli G, Ratz PH, Barbee RW, Klausner AP (2015) Acute length adaptation and adjustable preload in the human detrusor. Neurourol Urodyn. doi:10.1002/nau.22820
De Wachter S (2011) Afferent signaling from the bladder: species differences evident from extracellular recordings of pelvic and hypogastric nerves. Neurourol Urodyn 30(5):647–652. doi:10.1002/nau.21135
Rahnama’i MS, Van Koeveringe GA, Van Kerrebroeck PE (2013) Overactive bladder syndrome and the potential role of prostaglandins and phosphodiesterases: an introduction. Nephro-urol mon 5(4):934–945. doi:10.5812/numonthly.14087
Abrams P (2003) Describing bladder storage function: overactive bladder syndrome and detrusor overactivity. Urology 62(5 Suppl 2):28–37 (discussion 40–22)
Chacko S, Cortes E, Drake MJ, Fry CH (2014) Does altered myogenic activity contribute to OAB symptoms from detrusor overactivity? ICI-RS 2013. Neurourol Urodyn 33(5):577–580. doi:10.1002/nau.22599
Acknowledgements
Funding
Research funding for this study was provided by the Virginia Commonwealth University Presidential Research Quest Fund and National Institute of Health Grant R01DK101719.
Author’s contribution
AF Colhoun helped in protocol/project development, data collection, data analysis and manuscript writing/editing. JE Speich contributed to protocol/project development, data analysis and manuscript writing/editing. LF Cooley contributed to data collection and data analysis. ED Bell helped in data collection. RW Barbee helped in manuscript writing/editing. G Guruli contributed to data collection. PH Ratz contributed to protocol/project development and manuscript writing/editing. AP Klausner helped in protocol/project development, data analysis and manuscript writing/editing.
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Drs. Speich and Klausner report funding from the National Institutes of Health. Drs. Colhoun, Cooley, Bell, Barbee, Guruli and Ratz have no disclosures.
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All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki Declaration and its later amendments or comparable ethical standards. All experiments involving human bladder tissue were approved by the institutional review boards at Virginia Commonwealth University and the Hunter Holmes McGuire Veterans Affairs Medical Center. Informed consent was obtained from all patients involved in this study.
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Colhoun, A.F., Speich, J.E., Cooley, L.F. et al. Low amplitude rhythmic contraction frequency in human detrusor strips correlates with phasic intravesical pressure waves. World J Urol 35, 1255–1260 (2017). https://doi.org/10.1007/s00345-016-1994-0
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DOI: https://doi.org/10.1007/s00345-016-1994-0