
==== Front
World J Urol
World J Urol
World Journal of Urology
0724-4983
1433-8726
Springer Berlin Heidelberg Berlin/Heidelberg

39240342
5208
10.1007/s00345-024-05208-6
Research
Efficiency of HoLEP in patients with detrusor underactivity and renal dysfunction secondary to BPO
Yang Dengke
Sun Qian
Li Weiyuan
Wang Yibin
Qian Haining
http://orcid.org/0009-0009-5674-2330
Li Dong ld3649@shtrhospital.com

grid.459910.0 Department of Urology, Tongren Hospital, Shanghai Jiao Tong University School of Medicine, No. 1111 Xianxia Rd, Shanghai, China
6 9 2024
6 9 2024
2024
42 1 5098 3 2024
5 8 2024
© The Author(s) 2024
2024
https://creativecommons.org/licenses/by-nc-nd/4.0/ Open Access This article is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License, which permits any non-commercial use, sharing, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if you modified the licensed material. You do not have permission under this licence to share adapted material derived from this article or parts of it. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by-nc-nd/4.0/.
Purpose

The purpose of this study was to assess the bladder and renal functional outcomes of holmium laser enucleation of the prostate (HoLEP) in patients with benign prostatic obstruction (BPO) complicated by detrusor underactivity (DU) and secondary renal dysfunction.

Methods

Thirty-one patients were included in this prospective study. Eligible patients had urinary retention, a bladder outlet obstruction index (BOOI) greater than 40, a bladder contractility index (BCI) less than 100, abnormal renal function at the initial diagnosis (serum creatinine > 132 µmol/L) and a renal pelvis anteroposterior diameter (PRAPD) > 1.5 cm bilaterally. All patients underwent HoLEP in a routine manner and were evaluated preoperatively and at 1, 3 and 6 months after surgery. The baseline characteristics of the patients, perioperative data, postoperative outcomes and complications were assessed.

Results

Significant improvement was observed in the international prostate symptom score (IPSS), quality of life (QoL) score, maximal urinary flow rate (Qmax), post-void residual volume (PVR), Scr and RPAPD at the 6-month follow-up. Bladder wall thickness (BWT) exhibited a decreasing trend but did not significantly differ from the preoperative values. No grade 3 or higher adverse events occurred, and grade 3 and lower complications were treated conservatively. Three patients required reinsertion of indwelling catheters, and they were able to void spontaneously after two weeks of catheterisation training and medication treatment.

Conclusion

HoLEP is an effective treatment for men with BPO accompanied by DU and consequent renal function impairment. Patients are able to regain spontaneous voiding. Both bladder and renal functions were preserved and improved.

Keywords

Benign prostatic obstruction
Holmium laser enucleation of the prostate
Detrusor underactivity
Renal dysfunction
General Project of Shanghai Changning District Health Commission20214Y012 Yang Dengke Surface Project of Shanghai Health Commission202040140 Li Dong issue-copyright-statement© Springer-Verlag GmbH Germany, part of Springer Nature 2024
==== Body
pmcIntroduction

Lower urinary tract symptoms (LUTS) are common among adult males, significantly influence quality of life (QoL) and cause a substantial economic burden [1]. LUTS are conventionally associated with benign prostatic obstruction (BPO), which is commonly observed during the histological progression of benign prostatic hyperplasia (BPH) [2]. Nevertheless, an increasing number of studies have demonstrated that LUTS are often unrelated to the prostate but rather to bladder dysfunction, including detrusor underactivity (DU) [3]. Although the relationship between BPH and DU remains unclear, some studies have suggested that chronic urinary retention impairs detrusor muscle function, which gradually worsens over time and potentially results in renal function impairment [4].

The treatment of patients with severe DU remains controversial. Some physicians believe that operations can improve voiding conditions [5, 6], while others believe that surgical interventions have few benefits for BPH patients with severe DU [7], and conservative approaches such as indwelling catheterisation or bladder diversion procedures are preferred. Furthermore, DU with secondary renal dysfunction was historically considered a contraindication for transurethral resection of the prostate (TURP) in BPO patients [8].

Compared with alternative transurethral interventions for BPH, holmium laser enucleation of the prostate (HoLEP) exhibits superior effectiveness and leads to good long-term outcomes [9]. Nevertheless, the literature on the postoperative efficacy of HoLEP is limited regarding patients with BPO complicated by DU and resulting secondary damage. Thus, the aim of this study is to analyse postoperative changes in DU and renal dysfunction, particularly in these patients.

Materials and methods

Study design and population

In this prospective analysis, a total of 31 patients were assessed at Shanghai Tongren Hospital from January 2021 to July 2023. All patients had to meet the criteria of lower urinary tract obstruction, detrusor underactivity and renal dysfunction. Therefore, our inclusion criteria included urinary retention, a bladder outlet obstruction index (BOOI) greater than 40, a bladder contractility index (BCI) less than 100, abnormal renal function at the initial diagnosis (serum creatinine (Scr) > 132 µmol/L) and a renal pelvis anteroposterior diameter (PRAPD) > 1.5 cm bilaterally. In addition, the inclusion criteria also included a significant decrease in Scr and PRAPD two weeks after catheterisation. The aim of this study was to clarify whether DU and renal dysfunction are secondary to BPO rather than other causes. Patients with neurogenic bladder or prostate cancer or who had previously undergone transurethral surgery were excluded from the study. The ethics committee of our hospital approved the study prior to recruitment. Written informed consent was obtained.

The data were collected at enrolment and at the 1-month, 3-month, and 6-month follow-up. The evaluation of all the patients included the International Prostate Symptom Score (IPSS), quality of life (QoL), maximal urinary flow rate (Qmax), postvoid residual volume (PVR), bladder wall thickness (BWT), digital rectal examination (DRE), RPAPD measured by ultrasound, serum prostate specific antigen (PSA) level, and urodynamic study (UDS). The UDS was conducted to obtain various parameters, including the preoperative Qmax, bladder detrusor pressure at maximum urinary flow rate (PdetQmax), BCI, and BOOI. The calculation methods for the BCI and BOOI are as follows: BCI = PdetQmax + 5Qmax, BOOI = PdetQmax − 2Qmax. The UDS was performed 14 days after indwelling catheterisation and after renal function (Scr) stabilised. The catheter was then reinserted and retained until the day of surgery.

Surgical procedure

All HoLEP procedures were performed by the same experienced surgeon following the prostatic enucleation technique, as originally described by Gilling et al. [10, 11]. The instruments used were a Ho: YAG laser (P120Moses) with a 550 nm laser fibre, a 26-F continuous flow resectoscope, a 27-F nephroscope with a 5 mm working channel, a morcellator, normal saline irrigation and a video system. The laser settings were 40 Hz, 3 J for enucleation and 30 Hz, 1 J for haemostasis.

Statistical analysis

SPSS software was used to calculate the mean, standard deviation and rate for the clinical data. The data are presented as the means ± SDs or numbers (percentages). Due to the small sample size, we opted to use the Wilcoxon signed-rank test when comparing follow-up metrics with baseline data. A P value < 0.05 was considered significant.

Results

Based on the inclusion and exclusion criteria, 31 patients were enrolled in the study. All baseline characteristics and perioperative data are listed in Table 1.

Table 1 Characteristics of the patients included in the study

	Mean ± SD (range)	
Age (years)	73.74 ± 8.47	
Prostate volume (g)	84.39 ± 45.26	
PSA	6.53 ± 4.02	
IPSS	26.68 ± 4.08	
QoL	4.38 ± 0.66	
Qmax (mL/s)	4.39 ± 1.62	
PVR (mL)	839.94 ± 140.90	
Pdet-Qmax (cmH2O)	54.90 ± 5.96	
BCI	79.0 ± 13.02	
BOOI	45.17 ± 4.43	
BWT	4.01 ± 0.44	
Scr (µmol/L)	304.22 ± 162.39	
Scr after 2 weeks of catheterisation (µmol/L)	127.81 ± 33.66	
Left RPAPD (cm)	2.29 ± 0.35	
Right RPAPD (cm)	2.33 ± 0.46	
Left RPAPD after 2 weeks of catheterisation (cm)	0.69 ± 0.47	
Right RPAPD after 2 weeks of catheterisation (cm)	0.64 ± 0.37	
Enucleation time (min)	31.80 ± 9.25	
Morcellation time (min)	11.35 ± 6.49	
Enucleated tissue weight (g)	81.42 ± 36.07	
Indwelling catheter time (day)	5.25 ± 0.76	
Haemoglobin decrease (g/L)	6.84 ± 2.92	
PSA, prostate-specific antigen; IPSS, International Prostate Symptom Score; QoL, quality of life; Qmax, maximal urinary flow rate; PVR, post-void residual volume; Pdet-Qmax, detrusor pressure at maximum urinary flow rate; BCI, bladder contractility index; BOOI, bladder outlet obstruction index; BWT, bladder wall thickness; Scr, serum creatinine; RPAPD, renal pelvis anteroposterior diameter

Table 2 shows the functional outcomes in terms of IPSS, QoL, Qmax, PVR, BWT, Scr and RPAPD at 1, 3, and 6 months. Except BWT (p > 0.05), all the other parameters showed significant improvements compared to the baseline values at the 6-month follow-up (p < 0.05). Changes in the Qmax, PVR, and BWT observed during the follow-up assessments infer changes in bladder function, as shown in Fig. 1. The results showed a significant increase in the Qmax and a notable decrease in the PVR compared to the preoperative values. The change in BWT was not significant; however, a gradual decline in BWT was observed over time. Scr and RPAPD can serve as indicators of renal function changes, as shown in Fig. 2. The results showed a significant improvement in postoperative renal function for patients with no further deterioration observed over time.

Table 2 Comparison between baseline data and follow-up data up to 6 months

	Baseline	Follow-up data	P	
1 month	3 months	6 months	
IPSS	26.68 ± 4.08	9.26 ± 2.37	7.48 ± 1.64	6.87 ± 1.96	< 0.05	
QoL	4.39 ± 0.66	1.65 ± 0.82	1.52 ± 0.50	1.35 ± 0.60	< 0.05	
Qmax (mL/s)	4.39 ± 1.62	20.11 ± 4.81	19.65 ± 4.24	19.47 ± 3.56	< 0.05	
PVR (mL)	839.94 ± 140.90	38.55 ± 43.46	37.58 ± 43.23	38.71 ± 39.47	< 0.05	
BWT (mm)	4.01 ± 0.44	3.88 ± 0.43	3.612 ± 0.39	3.54 ± 0.40	> 0.05	
Scr (µmol/L)	304.22 ± 162.39	123.90 ± 36.80	117.613 ± 32.41	119.52 ± 30.18	< 0.05	
Left RPAPD (cm)	2.29 ± 0.35	0.48 ± 0.46	0.46 ± 0.47	0.43 ± 0.46	< 0.05	
Right PRAPD (cm)	2.33 ± 0.46	0.52 ± 0.41	0.46 ± 0.42	0.41 ± 0.42	< 0.05	
IPSS, International Prostate Symptom Score; QoL, quality of life; Qmax, maximal urinary flow rate; PVR, post-void residual volume; BWT, bladder wall thickness; Scr, serum creatinine; RPAPD, renal pelvis anteroposterior diameter

Fig. 1 Statistics of bladder functional outcomes up to 6 months. Significant changes (P < 0.05) between baseline and any follow-up time point are indicated by an asterisk (*). Qmax, maximal urinary flow rate; PVR, post-void residual volume; BWT, bladder wall thickness

Fig. 2 Statistics of renal functional outcomes up to 6 months. Significant changes (P < 0.05) between baseline and any follow-up time point are indicated by an asterisk (*). Scr, serum creatinine; RPAPD, renal pelvis anteroposterior diameter

Table 3 shows the incidence of complications according to the Clavien–Dindo system. There were no grade 3 or higher adverse events observed during the follow-up period. Two patients experienced febrile urinary tract infection and were treated with antibiotics. The incidences of haematuria and transient urge incontinence were 6.5% and 3.2%, respectively, and both conditions resolved with conservative treatments. Three patients were unable to void after catheter removal and required re-catheterisation. Following a two-week period of catheter clamping training and treatment with pyridostigmine, the patients were able to void spontaneously after the catheter was removed.

Table 3 Adverse events

Clavien‒Dindo	No. of patients with adverse events (%)	
Grade 1		
Haematuria	2 (6.5%)	
Transient urge incontinence	1 (3.2%)	
Grade 2		
Febrile urinary tract infection (temperature > 38.5)	2 (6.5%)	
Urinary retention	3 (9.7%)	

Discussion

The incidence of both BPH and DU increases with age [12], and DU may coexist with BPO and has been found in 25-37% of men with LUTS/BPH [13]. The relationship between BPO and DU remains unclear. Using rabbit models, Gosling et al. [14] demonstrated that prolonged partial bladder outflow obstruction is associated with a progressive decrease in smooth muscle contractility in the bladder. Levin et al. [15] reported that DU and bladder dysfunction may be secondary to BPO caused by BPH. Mirone et al. [16] also indicated that long-term BPO can result in bladder dysfunction and irreversible bladder damage. Prolonged BPO and DU can lead to chronic renal function failure [17]. Hence, some surgeons prefer earlier treatment for patients with moderate LUTS/BPH in cases of DU or renal dysfunction secondary to BPO [18].

It is common to encounter patients who present with DU and renal function impairment at their initial medical evaluation. However, there is limited research on this particular group of patients. This can be attributed to the relative consensus that surgical interventions are not suitable for patients who have severe bladder dysfunction with bladder contractility in a decompensated state, resulting in renal dysfunction. This is why conservative treatment approaches, such as long-term indwelling catheterisation or bladder diversion, are often preferred.

However, in our clinical practice, we have observed that a significant proportion of these patients were able to void spontaneously and that their renal function improved following HoLEP. Therefore, we initiated this prospective study focusing on patients with BPO complicated by DU and resulting renal function damage.

Except three patients who needed to have catheters reinserted, the remaining patients were able to void spontaneously. These patients exhibited a significant increase in their Qmax compared to their preoperative levels, and the majority of them experienced a reduction in PVR (PVR < 60 mL). There was a decreasing trend in BWT compared to the preoperative values; however, this was not statistically significant. Lee et al. [19] also reported a decrease in BWT after TURP, and a significant decrease in BWT was detected in the large prostate group after surgery. The decrease in BWT might become more prominent with a longer follow-up period. The patients exhibited a significant decrease in Scr levels compared to the preoperative values, and no clinical deterioration was observed. The results also indicated a significant decrease in the RPAPD compared to its preoperative values, which fell within the normal range. These findings indicate that renal function was preserved after HoLEP. From our series, we hypothesise that for urinary retention and the resulting renal dysfunction caused by both BPO and DU, the primary contributing factor in the majority of cases is BPO rather than DU; in other words, DU is secondary to BPO. If the obstruction is relieved, the DU can gradually improve, and renal function can be preserved.

We further analysed the clinical data of the three patients who needed re-catheterisation. These patients were ably after 2 weeks of catheter clamp training and treatment with oral pyridostigmine, but the PVR values remained between 60 mL and 200 mL. This finding suggested that the detrusor may have sustained irreversible damage in this subgroup, and the patients were unable to achieve complete bladder voiding despite the remission of BPO. However, the Qmax improved, patient quality of life significantly improved after discontinuation of indwelling catheters, and renal function also showed signs of recovery. This indicates that this subgroup of patients can benefit from HoLEP.

The results of other studies evaluating BPH surgery in patients with DU are mixed. Lebani et al. [20] reported that while there was minimal improvement in the Qmax after TURP in patients with DU than in men with normal bladder contraction, the IPSS and Qmax still significantly improved in DU patients. However, different findings are present in the literature. Abdelhakim et al. [21] reported significant improvements in the IPSS, detrusor contractility, and urine flow after TURP in 32 BPH patients with DU. Nevertheless, approximately 43% of these patients experienced postoperative urine retention and needed clean intermittent catheterisation at the 6-month follow-up. Although there is still debate regarding the incidence of postoperative urinary retention and the need for clean intermittent catheterisation, our results are consistent with a significant improvement in both the IPSS and the Qmax. This suggests that patients with DU can benefit from surgical intervention.

We believe that compared to other surgical modalities for BPH, HoLEP has two potential advantages for DU patients. First, according to the meta-analysis by Wroclawski et al. [22], which included three studies about HoLEP, the safety and efficacy of HoLEP for DU patients are comparable to those for patients with normal detrusor contractility, and there were no significant differences in the incidences of long-term complications. Second, with the anatomical enucleation of the prostate, HoLEP leads to maximal relief of obstruction, a reduction in outlet pressure, and a decrease in the risk of recurrence. Cho et al. [13] proposed that patients with BPH and DU may benefit from more complete removal of prostatic adenoma by HoLEP and greater baseline bladder contractility in terms of micturition, which supports our perspective.

The present study has several limitations. First, the strict inclusion criteria resulted in a small sample size. Additionally, the study lacked a control group, and it would be beneficial to include alternative surgical methods for comparison. Furthermore, postoperative follow-up did not include UDS values because patients refused to undergo invasive urodynamic testing during the follow-up period, and bladder function was indirectly assessed through the Qmax, PVR, and BWT [23, 24].

Conclusions

For patients with BPO complicated by DU and resulting renal dysfunction, HoLEP has the potential to restore patients’ ability to void spontaneously, protect bladder function and prevent further deterioration of renal function.

Abbreviations

HoLEP Holmium laser enucleation of the prostate

BPO Benign prostatic obstruction

DU Detrusor underactivity

BOOI Bladder Outlet Obstruction Index

BCI Bladder Contractility Index

Scr Serum Creatinine

RPAPD Renal pelvis anteroposterior diameter

IPSS International Prostate Symptom Score

QoL Quality of life

Qmax Maximal urinary flow rate

PVR Post-void residual volume

BWT Bladder wall thickness

LUTS Lower urinary tract symptoms

BPH Benign prostatic hyperplasia

TURP Transurethral Resection of the Prostate

DRE Digital rectal examination

UDS Urodynamic study

PdetQmax Detrusor pressure at maximum urinary flow rate

Acknowledgements

This work was supported by grants from the Surface Project of Shanghai Health Commission (202040140) and the General Project of Shanghai Changning District Health Commission (20214Y012).

Author contributions

Dengke Yang and Qian Sun: project development, data collection or management, data analysis, manuscript writing. Yibin Wang and Weiyuan Li: data collection or management. Haining Qian: project development. Dong Li: project development, manuscript editing and supervision. Dengke Yang and Qian Sun are first authors.

Data availability

The data that support the findings of this study are available from the corresponding author upon reasonable request.

Declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Publisher’s note

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

1. Gauhar V Technological innovations and evolving trends in endourological management for urolithiasis and benign prostatic hypertrophy World J Urol 2023 41 2879 2880 10.1007/s00345-023-04692-6 37897514
Gauhar V (2023) Technological innovations and evolving trends in endourological management for urolithiasis and benign prostatic hypertrophy. World J Urol 41:2879–2880. 10.1007/s00345-023-04692-637897514 10.1007/s00345-023-04692-6
2. Nguyen A-LV Verma I Ferreira R Nguyen D-D Zorn KC Bhojani N Lerner LB Gauhar V Chughtai B Elterman DS A scoping review of office-based prostatic stents: past, present, and future of true minimally invasive treatment of benign prostatic hyperplasia World J Urol 2023 41 2925 2932 10.1007/s00345-023-04508-7 37479913
Nguyen A-LV, Verma I, Ferreira R, Nguyen D-D, Zorn KC, Bhojani N, Lerner LB, Gauhar V, Chughtai B, Elterman DS (2023) A scoping review of office-based prostatic stents: past, present, and future of true minimally invasive treatment of benign prostatic hyperplasia. World J Urol 41:2925–2932. 10.1007/s00345-023-04508-737479913 10.1007/s00345-023-04508-7
3. Chapple CR Wein AJ Abrams P Dmochowski RR Giuliano F Kaplan SA McVary KT Roehrborn CG Lower urinary tract symptoms revisited: a broader clinical perspective Eur Urol 2008 54 563 569 10.1016/j.eururo.2008.03.109 18423969
Chapple CR, Wein AJ, Abrams P, Dmochowski RR, Giuliano F, Kaplan SA, McVary KT, Roehrborn CG (2008) Lower urinary tract symptoms revisited: a broader clinical perspective. Eur Urol 54:563–569. 10.1016/j.eururo.2008.03.10918423969 10.1016/j.eururo.2008.03.109
4. Thomas AW Cannon A Bartlett E Ellis-Jones J Abrams P The natural history of lower urinary tract dysfunction in men: minimum 10‐year urodynamic follow‐up of untreated bladder outlet obstruction BJU Int 2005 96 1301 1306 10.1111/j.1464-410x.2005.05815.x 16287449
Thomas AW, Cannon A, Bartlett E, Ellis-Jones J, Abrams P (2005) The natural history of lower urinary tract dysfunction in men: minimum 10‐year urodynamic follow‐up of untreated bladder outlet obstruction. BJU Int 96:1301–1306. 10.1111/j.1464-410x.2005.05815.x16287449 10.1111/j.1464-410x.2005.05815.x
5. Mitchell CR Mynderse LA Lightner DJ Husmann DA Krambeck AE Efficacy of holmium laser enucleation of the prostate in patients with non-neurogenic impaired bladder contractility: results of a prospective trial Urology 2014 83 428 432 10.1016/j.urology.2013.09.035 24231217
Mitchell CR, Mynderse LA, Lightner DJ, Husmann DA, Krambeck AE (2014) Efficacy of holmium laser enucleation of the prostate in patients with non-neurogenic impaired bladder contractility: results of a prospective trial. Urology 83:428–432. 10.1016/j.urology.2013.09.03524231217 10.1016/j.urology.2013.09.035
6. Tanabe T Ishizuka O Ichino M Ogawa T Imamura T Kurizaki Y Iijima K Nishizawa O Analysis of the pressure-flow study in weak detrusor patients with benign prostatic hypertrophy LUTS Low Urin Tract Symptoms 2011 3 109 112 10.1111/j.1757-5672.2011.00095.x 26676396
Tanabe T, Ishizuka O, Ichino M, Ogawa T, Imamura T, Kurizaki Y, Iijima K, Nishizawa O (2011) Analysis of the pressure-flow study in weak detrusor patients with benign prostatic hypertrophy. LUTS Low Urin Tract Symptoms 3:109–112. 10.1111/j.1757-5672.2011.00095.x26676396 10.1111/j.1757-5672.2011.00095.x
7. Machino R Kakizaki H Ameda K Shibata T Tanaka H Matsuura S Koyanagi T Detrusor instability with equivocal obstruction: a predictor of unfavorable symptomatic outcomes after transurethral prostatectomy Neurourol Urodyn 2002 21 444 449 10.1002/nau.10057 12232878
Machino R, Kakizaki H, Ameda K, Shibata T, Tanaka H, Matsuura S, Koyanagi T (2002) Detrusor instability with equivocal obstruction: a predictor of unfavorable symptomatic outcomes after transurethral prostatectomy. Neurourol Urodyn 21:444–449. 10.1002/nau.1005712232878 10.1002/nau.10057
8. Rassweiler J Teber D Kuntz R Hofmann R Complications of transurethral resection of the prostate (TURP)—incidence, management, and prevention Eur Urol 2006 50 969 980 10.1016/j.eururo.2005.12.042 16469429
Rassweiler J, Teber D, Kuntz R, Hofmann R (2006) Complications of transurethral resection of the prostate (TURP)—incidence, management, and prevention. Eur Urol 50:969–980. 10.1016/j.eururo.2005.12.04216469429 10.1016/j.eururo.2005.12.042
9. Abrams P Cardozo L Fall M Griffiths D Rosier P Ulmsten U Van Kerrebroeck P Victor A Wein A The standardisation of terminology in lower urinary tract function: report from the standardisation sub-committee of the International Continence Society Urology 2003 61 37 49 10.1016/s0090-4295(02)02243-4 12559262
Abrams P, Cardozo L, Fall M, Griffiths D, Rosier P, Ulmsten U, Van Kerrebroeck P, Victor A, Wein A (2003) The standardisation of terminology in lower urinary tract function: report from the standardisation sub-committee of the International Continence Society. Urology 61:37–49. 10.1016/s0090-4295(02)02243-412559262 10.1016/s0090-4295(02)02243-4
10. Gilling PJ Cass CB Cresswell MD Fraundorfer MR Holmium laser resection of the prostate: preliminary results of a new method for the treatment of benign prostatic hyperplasia Urology 1996 47 48 51 10.1016/s0090-4295(99)80381-1 8560662
Gilling PJ, Cass CB, Cresswell MD, Fraundorfer MR (1996) Holmium laser resection of the prostate: preliminary results of a new method for the treatment of benign prostatic hyperplasia. Urology 47:48–51. 10.1016/s0090-4295(99)80381-18560662 10.1016/s0090-4295(99)80381-1
11. Gilling PJ Cass CB Malcolm A Cresswell M Fraundorfer MR Kabalin JN Holmium laser resection of the prostate versus neodymium:yttrium-aluminum-garnet visual laser ablation of the prostate: a randomized prospective comparison of two techniques for laser prostatectomy Urology 1998 51 573 577 10.1016/s0090-4295(97)00642-0 9586609
Gilling PJ, Cass CB, Malcolm A, Cresswell M, Fraundorfer MR, Kabalin JN (1998) Holmium laser resection of the prostate versus neodymium:yttrium-aluminum-garnet visual laser ablation of the prostate: a randomized prospective comparison of two techniques for laser prostatectomy. Urology 51:573–577. 10.1016/s0090-4295(97)00642-09586609 10.1016/s0090-4295(97)00642-0
12. Osman NI Chapple CR Abrams P Dmochowski R Haab F Nitti V Koelbl H van Kerrebroeck P Wein AJ Detrusor underactivity and the underactive bladder: a new clinical entity? A review of current terminology, definitions, epidemiology, aetiology, and diagnosis Eur Urol 2014 65 389 398 10.1016/j.eururo.2013.10.015 24184024
Osman NI, Chapple CR, Abrams P, Dmochowski R, Haab F, Nitti V, Koelbl H, van Kerrebroeck P, Wein AJ (2014) Detrusor underactivity and the underactive bladder: a new clinical entity? A review of current terminology, definitions, epidemiology, aetiology, and diagnosis. Eur Urol 65:389–398. 10.1016/j.eururo.2013.10.01524184024 10.1016/j.eururo.2013.10.015
13. Cho MC Ha SB Park J Son H Oh S-J Kim SW Paick J-S Impact of detrusor underactivity on surgical outcomes of laser prostatectomy: comparison in serial 12-month follow-up outcomes between potassium-titanyl-phosphate photoselective vaporization of the prostate (PVP) and holmium laser enucleation of the prostate (HoLEP) Urology 2016 91 158 166 10.1016/j.urology.2015.11.052 26879733
Cho MC, Ha SB, Park J, Son H, Oh S-J, Kim SW, Paick J-S (2016) Impact of detrusor underactivity on surgical outcomes of laser prostatectomy: comparison in serial 12-month follow-up outcomes between potassium-titanyl-phosphate photoselective vaporization of the prostate (PVP) and holmium laser enucleation of the prostate (HoLEP). Urology 91:158–166. 10.1016/j.urology.2015.11.05226879733 10.1016/j.urology.2015.11.052
14. Gosling JA Kung LS Dixon JS Horan P Whitbeck C Levin RM Correlation between the structure and function of the rabbit urinary bladder following partial outlet obstruction J Urol 2000 163 1349 1356 10.1016/s0022-5347(05)67776-2 10737542
Gosling JA, Kung LS, Dixon JS, Horan P, Whitbeck C, Levin RM (2000) Correlation between the structure and function of the rabbit urinary bladder following partial outlet obstruction. J Urol 163:1349–1356. 10.1016/s0022-5347(05)67776-210737542 10.1016/s0022-5347(05)67776-2
15. Levin RM, Haugaard N, O’Connor L, Buttyan R, Das A, Dixon JS, Gosling JA (2000) Obstructive response of human bladder to BPH vs. rabbit bladder response to partial outlet obstruction: a direct comparison. Neurourol Urodyn 19:609–629. 10.1002/1520-6777(2000)19:5%3C609::aid-nau7%3E3.3.co;2-8
16. Mirone V Imbimbo C Longo N Fusco F The detrusor muscle: an innocent victim of bladder outlet obstruction Eur Urol 2007 51 57 66 10.1016/j.eururo.2006.07.050 16979287
Mirone V, Imbimbo C, Longo N, Fusco F (2007) The detrusor muscle: an innocent victim of bladder outlet obstruction. Eur Urol 51:57–66. 10.1016/j.eururo.2006.07.05016979287 10.1016/j.eururo.2006.07.050
17. Chapple CR Osman NI Birder L van Koeveringe GA Oelke M Nitti VW Drake MJ Yamaguchi O Abrams P Smith PP The underactive bladder: a new clinical concept? Eur Urol 2015 68 351 353 10.1016/j.eururo.2015.02.030 25770481
Chapple CR, Osman NI, Birder L, van Koeveringe GA, Oelke M, Nitti VW, Drake MJ, Yamaguchi O, Abrams P, Smith PP (2015) The underactive bladder: a new clinical concept? Eur Urol 68:351–353. 10.1016/j.eururo.2015.02.03025770481 10.1016/j.eururo.2015.02.030
18. Tao Y-C Wei Z-W Liu C Gu M Chen Q Chen Y-B Wang Z Better timing for HoLEP: a retrospective analysis of patients treated with HoLEP over a 10-year period with a 1-year follow-up Asian J Androl 2023 25 281 285 10.4103/aja202224 35532559
Tao Y-C, Wei Z-W, Liu C, Gu M, Chen Q, Chen Y-B, Wang Z (2023) Better timing for HoLEP: a retrospective analysis of patients treated with HoLEP over a 10-year period with a 1-year follow-up. Asian J Androl 25:281–285. 10.4103/aja20222435532559 10.4103/aja202224
19. Lee H Choo M Kim M Cho SY Lee SB Jeong H Son H Changes in bladder wall thickness and detrusor wall thickness after surgical treatment of benign prostatic enlargement in patients with lower urinary tract symptoms: a preliminary report Korean J Urol 2014 55 47 51 10.4111/kju.2014.55.1.47 24466397
Lee H, Choo M, Kim M, Cho SY, Lee SB, Jeong H, Son H (2014) Changes in bladder wall thickness and detrusor wall thickness after surgical treatment of benign prostatic enlargement in patients with lower urinary tract symptoms: a preliminary report. Korean J Urol 55:47–51. 10.4111/kju.2014.55.1.4724466397 10.4111/kju.2014.55.1.47
20. Lebani BR Barcelos ADS Gouveia DSES Girotti ME Remaille EP Skaff M Almeida FG The role of transurethral resection of prostate (TURP) in patients with underactive bladder: 12 months follow-up in different grades of detrusor contractility Prostate 2023 83 857 862 10.1002/pros.24526 36945749
Lebani BR, Barcelos ADS, Gouveia DSES, Girotti ME, Remaille EP, Skaff M, Almeida FG (2023) The role of transurethral resection of prostate (TURP) in patients with underactive bladder: 12 months follow-up in different grades of detrusor contractility. Prostate 83:857–862. 10.1002/pros.2452636945749 10.1002/pros.24526
21. Abdelhakim MA Rammah A Abozamel AH El-Sheikh MG Abdelazeem MS Abdallah SM Abdelaziz AY Does detrusor underactivity affect the results of transurethral resection of prostate? Int Urol Nephrol 2020 53 199 204 10.1007/s11255-020-02669-7 33074461
Abdelhakim MA, Rammah A, Abozamel AH, El-Sheikh MG, Abdelazeem MS, Abdallah SM, Abdelaziz AY (2020) Does detrusor underactivity affect the results of transurethral resection of prostate? Int Urol Nephrol 53:199–204. 10.1007/s11255-020-02669-733074461 10.1007/s11255-020-02669-7
22. Wroclawski ML Takemura LS Santos HOD Heldwein FL Gauhar V Lim EJ Law YXT Teoh JYC Herrmann TRW Castellani D Functional and safety outcomes after benign prostatic enlargement surgeries in men with detrusor underactivity compared with normal detrusor contractility: systematic review and meta-analysis Neurourol Urodyn 2023 43 126 143 10.1002/nau.25336 38010924
Wroclawski ML, Takemura LS, Santos HOD, Heldwein FL, Gauhar V, Lim EJ, Law YXT, Teoh JYC, Herrmann TRW, Castellani D (2023) Functional and safety outcomes after benign prostatic enlargement surgeries in men with detrusor underactivity compared with normal detrusor contractility: systematic review and meta-analysis. Neurourol Urodyn 43:126–143. 10.1002/nau.2533638010924 10.1002/nau.25336
23. Luo F Sun H-H Su Y-H Zhang Z-H Wang Y-S Zhao Z Li J Assessment of noninvasive predictors of bladder detrusor underactivity in BPH/LUTs patients Int Urol Nephrol 2017 49 787 792 10.1007/s11255-017-1539-5 28204989
Luo F, Sun H-H, Su Y-H, Zhang Z-H, Wang Y-S, Zhao Z, Li J (2017) Assessment of noninvasive predictors of bladder detrusor underactivity in BPH/LUTs patients. Int Urol Nephrol 49:787–792. 10.1007/s11255-017-1539-528204989 10.1007/s11255-017-1539-5
24. Ding Z Wang H Zhang W Hu H Wang Q Xu K Bladder wall thickness measured by CT can predict bladder outlet obstruction in men: a retrospective cohort study Int Urol Nephrol 2022 55 43 49 10.1007/s11255-022-03361-8 36103042
Ding Z, Wang H, Zhang W, Hu H, Wang Q, Xu K (2022) Bladder wall thickness measured by CT can predict bladder outlet obstruction in men: a retrospective cohort study. Int Urol Nephrol 55:43–49. 10.1007/s11255-022-03361-836103042 10.1007/s11255-022-03361-8
