Laparoscopic partial nephrectomy with intra-arterial cold perfusion. What can go wrong?

Introduction. In kidney masses of a high nephrometric index, a variant of renal ischemia is mostly needed, and to increase the time of compression of the renal artery, the cold renal ischemia may be relevant. Advantages of intra-arterial cold perfusion (IACP) are: good visualization and uniform cooling of the entire thickness of the renal parenchyma. This approach is not without its own set of challenges and potential complications during and after surgery. Purpose: to describe complications during kidney resection under IACP and options for their resolution with the practical recommendations based on literature data and clinical cases from our center. Material and Methods. The study included 14 patients with kidney masses of a high nephrometric index (RENAL 10 or more), who underwent kidney resections as an experimental technique under IACP from 2021 to 2024 at P.A. Hertzen Moscow Cancer Research Institute. Results. We identified both intra- and postoperative complications in 6 cases: perforation of the renal artery (n=1), brachial artery thrombosis (n=1), thrombosis of the renal artery (n=1), air embolism of segmental branches of the renal artery (n=2), urine leakage (n=1). Conclusion. The IACP-associated intraoperative complications in our cohort diminished over time as familiarity with the technique improved. The IACP is workable, efficient, and holds promise, indicating its appropriateness for large, well-equipped centers. In patients with just one functioning kidney and high nephrometric index masses needing prolonged ischemia during removal, this technique could become a lifesaving option as expertise grows.

1. Ferlay J., Colombet M., Soerjomataram I., Dyba T., Randi G., Bettio M., Gavin A., Visser O., Bray F. Cancer incidence and mortality patterns in Europe: Estimates for 40 countries and 25 major cancers in 2018. Eur J Cancer. 2018; 103: 356–87. doi: 10.1016/j.ejca.2018.07.005.

2. Capitanio U., Bensalah K., Bex A., Boorjian S.A., Bray F., Coleman J., Gore J.L., Sun M., Wood C., Russo P. Epidemiology of Renal Cell Carcinoma. Eur Urol. 2019; 75(1): 74–84. doi: 10.1016/j.eururo.2018.08.036.

3. Sung H., Ferlay J., Siegel R.L., Laversanne M., Soerjomataram I., Jemal A., Bray F. Global Cancer Statistics 2020: GLOBOCAN Estimates of Incidence and Mortality Worldwide for 36 Cancers in 185 Countries. CA Cancer J Clin. 2021; 71(3): 209–49. doi: 10.3322/caac.21660.

4. Ferlay J., Ervik M., Lam F., Laversanne M., Colombet M., Mery L., Piñeros M., Znaor A., Soerjomataram I. Global Cancer Observatory: Cancer Today [Internet]. Lyon, France: International Agency for Research on Cancer. [cited 01.09.2024]. URL: https://gco.iarc.who.int/today.

5. Linehan W.M., Zbar B. Focus on kidney cancer. Cancer Cell. 2004; 6(3): 223–28. doi: 10.1016/j.ccr.2004.09.006.

6. Thompson R.H., Boorjian S.A., Lohse C.M., Leibovich B.C., Kwon E.D., Cheville J.C., Blute M.L. Radical nephrectomy for pT1a renal masses may be associated with decreased overall survival compared with partial nephrectomy. J Urol. 2008; 179(2): 468–71. doi: 10.1016/j.juro.2007.09.077.

7. van Poppel H., Da Pozzo L., Albrecht W., Matveev V., Bono A., Borkowski A., Colombel M., Klotz L., Skinner E., Keane T., Marreaud S., Collette S., Sylvester R. A prospective, randomised EORTC intergroup phase 3 study comparing the oncologic outcome of elective nephronsparing surgery and radical nephrectomy for low-stage renal cell carcinoma. Eur Urol. 2011; 59(4): 543–52. doi: 10.1016/j.eururo.2010.12.013.

8. Kates M., Badalato G.M., Pitman M., McKiernan J.M. Increased risk of overall and cardiovascular mortality after radical nephrectomy for renal cell carcinoma 2 cm or less. J Urol. 2011; 186(4): 1247–53. doi: 10.1016/j.juro.2011.05.054.

9. Miller D.C., Schonlau M., Litwin M.S., Lai J., Saigal C.S.; Urologic Diseases in America Project. Renal and cardiovascular morbidity after partial or radical nephrectomy. Cancer. 2008; 112(3): 511–20. doi: 10.1002/cncr.23218.

10. Huang W.C., Elkin E.B., Levey A.S., Jang T.L, Russo P. Partial nephrectomy versus radical nephrectomy in patients with small renal tumors--is there a difference in mortality and cardiovascular outcomes? J Urol. 2009; 181(1): 55–61. doi: 10.1016/j.juro.2008.09.017.

11. Scosyrev E., Messing E.M., Sylvester R., Campbell S., van Poppel H. Renal function after nephron-sparing surgery versus radical nephrectomy: results from EORTC randomized trial 30904. Eur Urol. 2014; 65(2): 372–77. doi: 10.1016/j.eururo.2013.06.044.

12. Capitanio U., Terrone C., Antonelli A., Minervini A., Volpe A., Furlan M., Matloob R., Regis F., Fiori C., Porpiglia F., Di Trapani E., Zacchero M., Serni S., Salonia A., Carini M., Simeone C., Montorsi F., Bertini R. Nephron-sparing techniques independently decrease the risk of cardiovascular events relative to radical nephrectomy in patients with a T1a-T1b renal mass and normal preoperative renal function. Eur Urol. 2015; 67(4): 683–89. doi: 10.1016/j.eururo.2014.09.027.

13. MacLennan S., Imamura M., Lapitan M. C., Omar M. I., Lam T.B., Hilvano-Cabungcal A.M., Royle P., Stewart F., MacLennan G., MacLennan S.J., Dahm P., Canfield S.E., McClinton S., Griffiths T.R., Ljungberg B., N’Dow J.; UCAN Systematic Review Reference Group; EAU Renal Cancer Guideline Panel. Systematic review of perioperative and quality-of-life outcomes following surgical management of localised renal cancer. Eur Urol. 2012; 62(6): 1097–117. doi: 10.1016/j.eururo.2012.07.028.

14. Huang W.C., Levey A.S., Serio A.M., Snyder M., Vickers A.J., Raj G.V., Scardino P.T., Russo P. Chronic kidney disease after nephrectomy in patients with renal cortical tumours: a retrospective cohort study. Lancet Oncol. 2006; 7(9): 735–40. doi: 10.1016/S1470-2045(06)70803-8.

15. Ljungberg B., Albiges L., Abu-Ghanem Y., Bedke J., Capitanio U., Dabestani S., Fernández-Pello S., Giles R.H., Hofmann F., Hora M., Klatte T., Kuusk T., Lam T.B., Marconi L., Powles T., Tahbaz R., Volpe A., Bex A. European Association of Urology Guidelines on Renal Cell Carcinoma: The 2022 Update. Eur Urol. 2022; 82(4): 399–410. doi: 10.1016/j.eururo.2022.03.006.

16. Campbell S.C., Clark P.E., Chang S.S., Karam J.A., Souter L., Uzzo R.G. Renal Mass and Localized Renal Cancer: Evaluation, Management, and Follow-Up: AUA Guideline: Part I. J Urol. 2021; 206(2): 199–208. doi: 10.1097/JU.0000000000001911.

17. Gill I.S., Patil M.B., Abreu A.L., Ng C., Cai J., Berger A., Eisenberg M.S., Nakamoto M., Ukimura O., Goh A.C., Thangathurai D., Aron M., Desai M.M. Zero ischemia anatomical partial nephrectomy: a novel approach. J Urol. 2012; 187(3): 807–14. doi: 10.1016/j.juro.2011.10.

18. Desai M.M., Gill I.S., Ramani A.P., Spaliviero M., Rybicki L., Kaouk J.H. The impact of warm ischaemia on renal function after laparoscopic partial nephrectomy. BJU Int. 2005; 95(3): 377–83. doi: 10.1111/j.1464-410X.2005.05304.x.

19. Kallingal G.J., Weinberg J.M., Reis I.M., Nehra A., Venkatachalam M.A., Parekh D.J. Long-term response to renal ischaemia in the human kidney after partial nephrectomy: results from a prospective clinical trial. BJU Int. 2016; 117(5): 766–74. doi: 10.1111/bju.13192.

20. Zhang Z., Zhao J., Zabell J., Remer E., Li J., Campbell J., Dong W., Palacios D.A., Patel T., Demirjian S., Campbell S.C. Proteinuria in Patients Undergoing Renal Cancer Surgery: Impact on Overall Survival and Stability of Renal Function. Eur Urol Focus. 2016; 2(6): 616–22. doi: 10.1016/j.euf.2016.01.003.

21. Thompson R.H., Lane B.R., Lohse C.M., Leibovich B.C., Fergany A., Frank I., Gill I.S., Blute M.L,. Campbell S.C. Every minute counts when the renal hilum is clamped during partial nephrectomy. Eur Urol. 2010; 58(3): 340–45. doi: 10.1016/j.eururo.2010.05.047.

22. Mir M.C., Ercole C., Takagi T., Zhang Z., Velet L., Remer E.M., Demirjian S., Campbell S.C. Decline in renal function after partial nephrectomy: etiology and prevention. J Urol. 2015; 193(6): 1889–98. doi: 10.1016/j.juro.2015.01.093.

23. Simmons M.N., Hillyer S.P., Lee B.H., Fergany A.F., Kaouk J., Campbell S.C. Functional recovery after partial nephrectomy: effects of volume loss and ischemic injury. J Urol. 2012; 187(5): 1667–73. doi: 10.1016/j.juro.2011.12.068.

24. Mir M.C., Campbell R.A., Sharma N., Remer E.M., Simmons M.N., Li J., Demirjian S., Kaouk J., Campbell S.C. Parenchymal volume preservation and ischemia during partial nephrectomy: functional and volumetric analysis. Urology. 2013; 82(2): 263–68. doi: 10.1016/j.urology.2013.03.068.

25. Anderson B.G., Potretzke A.M., Du K., Vetter J.M., Bergeron K., Paradis A.G., Figenshau R.S. Comparing Off-clamp and On-clamp Robotassisted Partial Nephrectomy: A Prospective Randomized Trial. Urology. 2019; 126: 102–9. doi: 10.1016/j.urology.2018.11.053.

26. Kutikov A., Uzzo R.G. The R.E.N.A.L. nephrometry score: a comprehensive standardized system for quantitating renal tumor size, location and depth. J Urol. 2009; 182(3): 844–53. doi: 10.1016/j.juro.2009.05.035.

27. Maathuis M.H., Leuvenink H.G., Ploeg R.J. Perspectives in organ preservation. Transplantation. 2007; 83(10): 1289–98. doi: 10.1097/01.tp.0000265586.66475.cc.

28. Steffens J., Humke U., Ziegler M., Siemer S. Partial nephrectomy with perfusion cooling for imperative indications: a 24-year experience. BJU Int. 2005; 96(4): 608–11. doi: 10.1111/j.1464-410X.2005.05693.x.

29. Novick A.C. Renal hypothermia: in vivo and ex vivo. Urol Clin North Am. 1983; 10(4): 637–44.

30. Weld K.J., Koziol S., Montiglio C., Sorenson P., Cespedes R.D., Bishoff J.T. Feasibility of laparoscopic renal cooling with near-freezing saline irrigation delivered with a standard irrigator aspirator. Urology. 2007; 69(3): 465–68. doi: 10.1016/j.urology.2006.12.002.

31. Janetschek G., Abdelmaksoud A., Bagheri F., Al-Zahrani H., Leeb K., Gschwendtner M. Laparoscopic partial nephrectomy in cold ischemia: renal artery perfusion. J Urol. 2004; 171(1): 68–71. doi: 10.1097/01.ju.0000101040.13244.c4.

32. Beri A., Lattouf J. B., Deambros O., Grüll M., Gschwendtner M., Ziegerhofer J., Leeb K., Janetschek G. Partial nephrectomy using renal artery perfusion for cold ischemia: functional and oncologic outcomes. J Endourol. 2008; 22(6): 1285–90. doi: 10.1089/end.2008.0152.

33. De Backer P., Vangeneugden J., Berquin C., Vermijs S., Dekuyper P., Mottrie A., Debbaut C., Quackels T., van Praet C., Decaestecker K. Robotassisted Partial Nephrectomy Using Intra-arterial Renal Hypothermia for Highly Complex Endophytic or Hilar Tumors: Case Series and Description of Surgical Technique. Eur Urol Open Sci. 2023; 58: 19–27. doi: 10.1016/j.euros.2023.10.004.

34. Zhu C., Yin H., Zhao S., Ma Y., Sun Z., Zhu M., Du Z., Yang T. Clinical study of renal artery cold perfusion combined with laparoscopic nephron retention in the treatment of complex renal angiomyolipoma. Front Oncol. 2023; 13: 1220380. doi: 10.3389/fonc.2023.1220380.

35. Lu Q., Zhao X., Ji C., Guo S., Qiu X., Liu G., Zhang S., Li X., Zhang G., Zhang X., Guo H. Functional and oncologic outcomes of robotassisted simple enucleation with and without renal arterial cold perfusion in complex renal tumors: a propensity score-matched analysis. BMC Urol. 2021; 21(1): 2. doi: 10.1186/s12894-020-00771-7.

36. Liu F., Yuan H., Li X., Ma X., Wang M. Application of Hypothermic Perfusion via a Renal Artery Balloon Catheter During Robot-assisted Partial Nephrectomy and Effect on Renal Function. Acad Radiol. 2019; 26(8): 196–201. doi: 10.1016/j.acra.2018.09.024.

37. Marley C.S., Siegrist T., Kurta J., O’Brien F., Bernstein M., Solomon S., Coleman J.A. Cold intravascular organ perfusion for renal hypothermia during laparoscopic partial nephrectomy. J Urol. 2011; 185(6): 2191–95. doi: 10.1016/j.juro.2011.02.013.

38. Mendez P., Lineros R., Ospina D., Ringa M., Eyheremendy E. Endovascular Management of Iatrogenic Renal Vascular Injuries: Case Series and Systematic Review. Arch Esp Urol. 2022; 75(6): 524–31. doi: 10.37554/es-j.arch.esp.urol-20210515-3507-27.

39. Aykan S., Temiz M.Z., Ulus I., Yilmaz M., Gonultas S., Suzan S., Semercioz A., Muslumanoglu A.Y. The Use of Three Different Hemostatic Agents during Laparoscopic Partial Nephrectomy: A Comparison of Surgical and Early Renal Functional Outcomes. Eurasian J Med. 2019; 51(2): 160–64. doi: 10.5152/eurasianjmed.2018.18293.

40. Shen H.L., Chueh S.C., Lai M.K., Wu C.H., Huang C.C., Tsang Y.M., Chuang C.C., Lai M.C., Yu H.J. Balloon occlusion and hypothermic perfusion of the renal artery in laparoscopic partial nephectomy. Int J Urol. 2008; 15(11): 967–70. doi: 10.1111/j.1442-2042.2008.02158.x.

41. Marberger M., Günther R., Mayer E.J., Wiestler M. A simple method for in situ preservation of the ischemic kidney during renal surgery. Invest Urol. 1976; 14(3): 191–93.

42. Marberger M., Georgi M., Guenther R., Hohenfellner R. Simultaneous balloon occlusion of the renal artery and hypothermic perfusion in in situ surgery of the kidney. J Urol. 1978; 119(4): 463–67. doi: 10.1016/s0022-5347(17)57517-5.