Skip to main content
Log in

Bladder augmentation from an insider’s perspective: a review of the literature on microcirculatory studies

  • Urology - Review
  • Published:
International Urology and Nephrology Aims and scope Submit manuscript

Abstract

Augmentation cystoplasty is an exemplary multiorgan intervention in urology which is particularly associated with microvascular damage. Our aim was to review the available intravital imaging techniques and data obtained from clinical and experimental microcirculatory studies involving the most important donor organs applied in bladder augmentation. Although numerous direct or indirect methods are available to assess the condition of microvessels the implementation of microcirculatory diagnostic methods in humans is still challenging and the assessment of organ microcirculation in the operating theatre has limitations. Nevertheless, preclinical studies generally report good internal validity and although prospective human protocols with reduced variability are needed, a possible positive impact of microcirculatory diagnostics on the clinical outcomes of urologic surgery can be anticipated.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

Availability of data and material

Not applicable.

Code availability

Not applicable.

References

  1. Jednak R (2014) The evolution of bladder augmentation: from creating a reservoir to reconstituting an organ. Front Pediatr 2:10

    Article  PubMed  PubMed Central  Google Scholar 

  2. Kardos DJ, Kereskai L, Tornoczky T, Farkas K, Davidovics A, Farkas A et al (2019) Re-evaluation of histological findings after colocystoplasty and gastrocystoplasty. J Pediatr Urol 15(6):651.e1-651.e8

    Article  Google Scholar 

  3. Bertschy C, Bawab F, Liard A, Valioulis I, Mitrofanoff P (2000) Enterocystoplasty complications in children. A study of 30 cases. Eur J Pediatr Surg 10(1):30–34. https://doi.org/10.1055/s-2008-1072319

    Article  CAS  PubMed  Google Scholar 

  4. DeFoor W, Tackett L, Minevich E, Wacksman J, Sheldon C (2003) Risk factors for spontaneous bladder perforation after augmentation cystoplasty. Urology 62(4):737–741. https://doi.org/10.1016/s0090-4295(03)00678-2

    Article  PubMed  Google Scholar 

  5. Metcalfe PD, Rink RC (2007) Bladder augmentation: complications in the pediatric population. Curr Urol Rep 8(2):152–156. https://doi.org/10.1007/s11934-007-0065-x

    Article  PubMed  Google Scholar 

  6. Shekarriz B, Upadhyay J, Demirbilek S, Barthold JS, González R (2000) Surgical complications of bladder augmentation: comparison between various enterocystoplasties in 133 patients. Urology 55(1):123–128. https://doi.org/10.1016/s0090-4295(99)00443-4

    Article  CAS  PubMed  Google Scholar 

  7. Slaton JW, Kropp KA (1994) Conservative management of suspected bladder rupture after augmentation enterocystoplasty. J Urol 152(2 Pt 2):713–715. https://doi.org/10.1016/s0022-5347(17)32688-5

    Article  CAS  PubMed  Google Scholar 

  8. Bajory Z, Szabó A, Pajor L, Tiszlavicz L, Boros M (2001) Intravital microscopic assessment of pressure induced microcirculatory changes after enterocystoplasty in rats. J Urol 165(4):1279–1282

    Article  CAS  PubMed  Google Scholar 

  9. Crane JM, Scherz HS, Billman GF, Kaplan GW (1991) Ischemic necrosis: a hypothesis to explain the pathogenesis of spontaneously ruptured enterocystoplasty. J Urol 146(1):141–144. https://doi.org/10.1016/s0022-5347(17)37733-9

    Article  CAS  PubMed  Google Scholar 

  10. Elder JS, Snyder HM, Hulbert WC, Duckett JW (1988) Perforation of the augmented bladder in patients undergoing clean intermittent catheterization. J Urol 140(5 Pt 2):1159–1162. https://doi.org/10.1016/s0022-5347(17)41988-4

    Article  CAS  PubMed  Google Scholar 

  11. Sheiner JR, Kaplan GW (1988) Spontaneous bladder rupture following enterocystoplasty. J Urol 140(5 Pt 2):1157–1158. https://doi.org/10.1016/s0022-5347(17)41987-2

    Article  CAS  PubMed  Google Scholar 

  12. Miodoński AJ, Litwin JA (1999) Microvascular architecture of the human urinary bladder wall: a corrosion casting study. Anat Rec 254(3):375–381. https://doi.org/10.1002/(SICI)1097-0185(19990301)254:3%3c375::AID-AR8%3e3.0.CO;2-R

    Article  PubMed  Google Scholar 

  13. Hossler F, Kao R (2007) Microvasculature of the urinary bladder of the dog: a study using vascular corrosion casting. Microsc Microanal 13(3):220–227. https://doi.org/10.1017/S1431927607070249

    Article  CAS  PubMed  Google Scholar 

  14. Kershen RT, Azadzoi KM, Siroky MB (2002) Blood flow, pressure and compliance in the male human bladder. J Urol 168(1):121–125. https://doi.org/10.1016/S0022-5347(05)64843-4

    Article  PubMed  Google Scholar 

  15. Nielsen KK (1995) Blood flow rate and total blood flow related to length density and total length of blood vessels in mini-pig urinary bladder after chronic outflow obstruction and after recovery from obstruction. Neurourol Urodyn 14(2):177–186. https://doi.org/10.1002/nau.1930140210

    Article  CAS  PubMed  Google Scholar 

  16. Yamaguchi O, Nomiya M, Andersson KE (2014) Functional consequences of chronic bladder ischemia. Neurourol Urodyn 33(1):54–58. https://doi.org/10.1002/nau.22517

    Article  PubMed  Google Scholar 

  17. Yuan Y, Duranceau A, Ferraro P, Martin J, Liberman M (2012) Vascular conditioning of the stomach before esophageal reconstruction by gastric interposition. Dis Esophagus 25(8):740–749. https://doi.org/10.1111/j.1442-2050.2011.01311.x

    Article  CAS  PubMed  Google Scholar 

  18. Akiyama S, Kodera Y, Sekiguchi H, Kasai Y, Kondo K, Ito K et al (1998) Preoperative embolization therapy for esophageal operation. J Surg Oncol 69:219–223. https://doi.org/10.1002/(SICI)1096-9098(199812)69:43.0.CO;2-7

    Article  CAS  PubMed  Google Scholar 

  19. Liebermann-Meffert DM, Meier R, Siewert JR (1992) Vascular anatomy of the gastric tube used for esophageal reconstruction. Ann Thorac Surg 54(6):1110–1115. https://doi.org/10.1016/0003-4975(92)90077-h

    Article  CAS  PubMed  Google Scholar 

  20. Ndoye JM, Dia A, Ndiaye A, Fall B, Diop M, Ndiaye A et al (2006) Arteriography of three models of gastric oesophagoplasty: the whole stomach, a wide gastric tube and a narrow gastric tube. Surg Radiol Anat 28(5):429–437. https://doi.org/10.1007/s00276-006-0129-5

    Article  PubMed  Google Scholar 

  21. Takeda FR, Cecconello I, Szachnowicz S, Tacconi MR, Gama-Rodrigues J (2005) Anatomic study of gastric vascularization and its relationship to cervical gastroplasty. J Gastrointest Surg 9(1):132–137. https://doi.org/10.1016/j.gassur.2004.03.006

    Article  PubMed  Google Scholar 

  22. Prasetya H, Jansen SM, Marquering HA, van Leeuwen TG, Gisbertz S, de Bruin DM et al (2019) Estimation of microvascular perfusion after esophagectomy: a quantitative model of dynamic fluorescence imaging. Med Biol Eng Comput 57(9):1889–1900. https://doi.org/10.1007/s11517-019-01994-z

    Article  PubMed  PubMed Central  Google Scholar 

  23. Urschel JD, Takita H, Antkowiak JG (1997) The effect of ischemic conditioning on gastric wound healing in the rat: implications for esophageal replacement with stomach. J Cardiovasc Surg 38(5):535–538

    CAS  Google Scholar 

  24. Mittermair C, Klaus A, Scheidl S, Maglione M, Hermann M, Margreiter R et al (2008) Functional capillary density in ischemic conditioning: implications for esophageal resection with the gastric conduit. Am J Surg 196(1):88–92. https://doi.org/10.1016/j.amjsurg.2007.07.025

    Article  PubMed  Google Scholar 

  25. Schilling MK, Mettler D, Redaelli C, Büchler MW (1997) Circulatory and anatomic differences among experimental gastric tubes as esophageal replacement. World J Surg 21(9):992–997. https://doi.org/10.1007/s002689900338

    Article  CAS  PubMed  Google Scholar 

  26. Schröder W, Beckurts KTE, Stähler D, Stützer H, Fischer JH, Hölscher AH (2002) Microcirculatory changes associated with gastric tube formation in the pig. Eur Surg Res 34:411–417. https://doi.org/10.1159/000065709

    Article  PubMed  Google Scholar 

  27. Ambrus R, Svendsen LB, Secher NH, Rünitz K, Frederiksen HJ, Svendsen MBS et al (2017) A reduced gastric corpus microvascular blood flow during Ivor-Lewis esophagectomy detected by laser speckle contrast imaging technique. Scand J Gastroenterol 52(4):455–461. https://doi.org/10.1080/00365521.2016.1265664

    Article  PubMed  Google Scholar 

  28. Bludau M, Vallböhmer D, Gutschow C, Hölscher AH, Schröder W (2008) Quantitative measurement of gastric mucosal microcirculation using a combined laser Doppler flowmeter and spectrophotometer. Dis Esophagus 21(7):668–672. https://doi.org/10.1111/j.1442-2050.2008.00856.x

    Article  CAS  PubMed  Google Scholar 

  29. Delko T, Hoffmann H, Kraljević M, Droeser RA, Rothwell L, Oertli D et al (2017) Intraoperative patterns of gastric microperfusion during laparoscopic sleeve gastrectomy. Obes Surg 27(4):926–932. https://doi.org/10.1007/s11695-016-2386-7

    Article  PubMed  Google Scholar 

  30. Cserni T, Cervellione RM, Hajnal D, Varga G, Kubiak R, Rakoczy G et al (2015) Alternative ileal flap for bladder augmentation if mesentery is short. J Pediatr Urol 11(2):64.e1–6. https://doi.org/10.1016/j.jpurol.2014.10.008

    Article  CAS  Google Scholar 

  31. Cervellione RM, Varga G, Hajnal D, Érces D, Kaszaki J, Harwood R et al (2016) Intestinal intramural vascular anastomoses. J Invest Surg 29(1):51–56. https://doi.org/10.3109/08941939.2015.1045106

    Article  PubMed  Google Scholar 

  32. Cervellione RM, Hajnal D, Varga G, Érces D, Kaszaki J, Keene D et al (2017) Mucosectomy impairs ileal microcirculation and results in flap contraction after experimental ileocystoplasty. J Pediatr Urol 13(1):81.e1-81.e5. https://doi.org/10.1016/j.jpurol.2016.11.007

    Article  Google Scholar 

  33. Urbán D, Marei MM, Hajnal D, Varga G, Érces D, Poles M et al (2020) Mucosectomy disrupting the enteric nervous system causes contraction and shrinkage of gastrointestinal flaps: potential implications for augmentation cystoplasty. J Pediatr Urol 16(1):20–26. https://doi.org/10.1016/j.jpurol.2019.08.019

    Article  PubMed  Google Scholar 

  34. Tavy A, Bruin A, Smits A, Boerma EC, Smits AB, Boerma EC et al (2020) Intestinal mucosal and serosal microcirculation at the planned anastomosis during abdominal surgery. Eur Surg Res 60:1–9. https://doi.org/10.1159/000505325

    Article  Google Scholar 

  35. De Bruin AFJ, Tavy ALM, van der Sloot K, Smits A, Ince C, Boerma EC et al (2018) Can sidestream dark field (SDF) imaging identify subtle microvascular changes of the bowel during colorectal surgery? Tech Coloproctol 22:793–800. https://doi.org/10.1007/s10151-018-1872-4

    Article  PubMed  Google Scholar 

  36. Wada T, Kawada K, Takahashi R, Yoshitomi M, Hida K, Hasegawa S et al (2017) ICG fluorescence imaging for quantitative evaluation of colonic perfusion in laparoscopic colorectal surgery. Surg Endosc 31(10):4184–4193. https://doi.org/10.1007/s00464-017-5475-3

    Article  PubMed  Google Scholar 

  37. Murray ACA, Chiuzan C, Kiran RP (2016) Risk of anastomotic leak after laparoscopic versus open colectomy. Surg Endosc 30(12):5275–5282. https://doi.org/10.1007/s00464-016-4875-0

    Article  PubMed  Google Scholar 

  38. Siegemund M, van Bommel J, Stegenga ME, Studer W, van Iterson M, Annaheim S et al (2010) Aortic cross-clamping and reperfusion in pigs reduces microvascular oxygenation by altered systemic and regional blood flow distribution. Anesth Analg 111(2):345–353

    Article  CAS  PubMed  Google Scholar 

  39. Jafari MD, Lee KH, Halabi WJ, Mills SD, Carmichael JC, Stamos MJ et al (2013) The use of indocyanine green fluorescence to assess anastomotic perfusion during robotic assisted laparoscopic rectal surgery. Surg Endosc 27:3003–3008. https://doi.org/10.1007/s00464-013-2832-8

    Article  PubMed  Google Scholar 

  40. Millan M, García-Granero E, Flor B, García-Botello S, Lledo S (2006) Early prediction of anastomotic leak in colorectal cancer surgery by intramucosal pH. Dis Colon Rectum 49(5):595–601. https://doi.org/10.1007/s10350-006-0504-7

    Article  PubMed  Google Scholar 

  41. Wu Z, Boersema GSA, Taha D, Fine I, Menon A, Kleinrensink GJ et al (2016) Postoperative hemodynamic index measurement with miniaturized dynamic light scattering predicts colorectal anastomotic healing. Surgical Innovation 23(2):115–123. https://doi.org/10.1177/1553350615618286

    Article  PubMed  Google Scholar 

  42. Turner A, Subramanian R, Thomas DFM, Hinley J, Abbas SK, Stahlschmidt J et al (2011) Transplantation of autologous differentiated urothelium in an experimental model of composite cystoplasty. Eur Urol 59(3):447–454. https://doi.org/10.1016/j.eururo.2010.12.004

    Article  PubMed  PubMed Central  Google Scholar 

  43. Jansen SM, De Bruin DM, van Berge Henegouwen MI, Strackee SD, Veelo DP et al (2018) Optical techniques for perfusion monitoring of the gastric tube after esophagectomy: a review of technologies and thresholds. Dis Esophagus. https://doi.org/10.1093/dote/dox161

    Article  PubMed  Google Scholar 

  44. De Bruin AFJ, Kornmann V, Sloot K, Vugt J, Gosselink MP, Smits A et al (2016) Sidestream dark field imaging of the serosal microcirculation during gastrointestinal surgery. Colorectal Dis 18(3):O103–O110. https://doi.org/10.1111/codi.13250

    Article  PubMed  Google Scholar 

  45. Laemmel E, Genet M, Le Goualher G, Perchant A, Le Gargasson J-F, Vicaut E (2004) Fibered confocal fluorescence microscopy (Cell-viZio) facilitates extended imaging in the field of microcirculation. A comparison with intravital microscopy. J Vasc Res 41(5):400–401. https://doi.org/10.1159/000081209

    Article  PubMed  Google Scholar 

  46. Diana M, Dallemagne B, Chung H, Halvax P, Agnus V, Soler L et al (2014) Probe-based confocal laser endomicroscopy and fluorescence-based enhanced reality for real-time assessment of intestinal microcirculation in a porcine model of sigmoid ischemia. Surg Endosc 28(11):3224–3233. https://doi.org/10.1007/s00464-014-3595-6

    Article  PubMed  Google Scholar 

  47. Kovács T, Varga G, Érces D, Tőkes T, Tiszlavicz L, Ghyczy M et al (2012) Dietary phosphatidylcholine supplementation attenuates inflammatory mucosal damage in a rat model of experimental colitis. Shock 38:177–185. https://doi.org/10.1097/SHK.0b013e31825d1ed0

    Article  CAS  PubMed  Google Scholar 

  48. Zhangyuanzhu L, Xiaobei L, Wei J, Dexin C, Weisheng C, Kai L et al (2019) (2019) Real-time in vivo optical biopsy using confocal laser endomicroscopy to evaluate distal margin in situ and determine surgical procedure in low rectal cancer. Surg endosc 33(7):2332–2338. https://doi.org/10.1007/s00464-018-6519-z

    Article  Google Scholar 

  49. Tian Y, Zheng Y, Teng G, Li J, Wang H (2019) Imbalanced mucosal microcirculation in the remission stage of ulcerative colitis using probe-based confocal laser endomicroscopy. BMC Gastroenterol 19(1):1–9. https://doi.org/10.1186/s12876-019-1037-6

    Article  CAS  Google Scholar 

  50. Lee J, Jeh SU, Koh DH, Chung DY, Kim MS, Goh HJ et al (2019) Probe-based confocal laser endomicroscopy during transurethral resection of bladder tumors improves the diagnostic accuracy and therapeutic efficacy. Ann Surg Oncol 26(4):1158–1165. https://doi.org/10.1245/s10434-019-07200-6

    Article  PubMed  PubMed Central  Google Scholar 

  51. Liem EIML, Freund JE, Savci-Heijink CD, de la Rosette JJ, Kamphuis GM, Baard J et al (2020) Validation of confocal laser endomicroscopy features of bladder cancer: the next step towards real-time histologic grading. Eur Urol Focus 6(1):81–87. https://doi.org/10.1016/j.euf.2018.07.012

    Article  PubMed  Google Scholar 

  52. Groner W, Winkelman JW, Harris AG, Ince C, Bouma GJ, Messmer K et al (1999) Orthogonal polarization spectral imaging: a new method for study of the microcirculation. Nat Med 5(10):1209–1212. https://doi.org/10.1038/13529

    Article  CAS  PubMed  Google Scholar 

  53. Van Elteren HA, Ince C, Tibboel D, Reiss IK, de Jonge RC (2015) Cutaneous microcirculation in preterm neonates: comparison between sidestream dark field (SDF) and incident dark field (IDF) imaging. J Clin Monit Comput 29(5):543–548. https://doi.org/10.1007/s10877-015-9708-5

    Article  PubMed  PubMed Central  Google Scholar 

  54. De Backer D, Hollenberg S, Boerma C, Goedhart P, Büchele G, Ospina-Tascon G et al (2007) How to evaluate the microcirculation: report of a round table conference. Crit Care 11(5):R101. https://doi.org/10.1186/cc6118

    Article  PubMed  PubMed Central  Google Scholar 

  55. Xu M, Wang LV (2006) Photoacoustic imaging in biomedicine. Rev Sci Instrum 77(4):041101

    Article  Google Scholar 

  56. Steinberg I, Huland DM, Vermesh O, Frostig HE, Tummers WS, Gambhir SS (2019) Photoacoustic clinical imaging. Photoacoustics 14:77–98. https://doi.org/10.1016/j.pacs.2019.05.001

    Article  PubMed  PubMed Central  Google Scholar 

  57. Schröder W, Stippel D, Gutschow C, Leers J, Hölscher AH (2004) Postoperative recovery of microcirculation after gastric tube formation. Langenbecks Arch Surg 389(4):267–271. https://doi.org/10.1007/s00423-004-0493-8

    Article  PubMed  Google Scholar 

  58. Hölscher AH, Schneider PM, Gutschow C, Schröder W (2007) Laparoscopic ischemic conditioning of the stomach for esophageal replacement. Ann Surg 245(2):241–246. https://doi.org/10.1097/01.sla.0000245847.40779.10

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

Gabriella Varga and Dániel Érces contributed equally to the paper. The study was supported by Economic Development and Innovation Operational Programme GINOP-2.3.2-15-2016-00034.

Funding

The study was supported by the Economic Development and Innovation Operational Programme GINOP-2.3.2-15-2016-00034.

Author information

Authors and Affiliations

Authors

Contributions

DU wrote and edited the manuscript and did literature search; TC edited and critically revised the manuscript; MB did literature search and critically revised the manuscript; ÁJ critically revised the manuscript; DE wrote, edited and critically revised the manuscript; GV initiated the project, did literature search, wrote and critically revised the manuscript.

Corresponding author

Correspondence to Gabriella Varga.

Ethics declarations

Conflict of interest

The authors have no conflicts of interest to declare that are relevant to the content of this article.

Ethics approval

Not applicable.

Consent to participate

Not applicable.

Consent for publication

Not applicable.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Urbán, D., Cserni, T., Boros, M. et al. Bladder augmentation from an insider’s perspective: a review of the literature on microcirculatory studies. Int Urol Nephrol 53, 2221–2230 (2021). https://doi.org/10.1007/s11255-021-02971-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11255-021-02971-y

Keywords

Navigation