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Observation and Mechanism Study of Bladder Wound Healing After Transurethral Holmium Laser Resection of Bladder Tumor

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Observation and Mechanism Study of Bladder Wound Healing After Transurethral Holmium Laser Resection of Bladder Tumor Lasers in Medical Science (2019) 34:1217–1227 https://doi.org/10.1007/s10103-018-02713-0 ORIGINAL ARTICLE Observation and mechanism study of bladder wound healing after transurethral holmium laser resection of bladder tumor Sha Han1 & Kai Dong2 & Mengjun Shen2 & Xingjie Wang2 & Wanzi Jiang3 & Wei Zhao2,4 & Dongliang Xu2,4,5 Received: 8 August 2018 /Accepted: 26 December 2018 /Published online: 22 February 2019 # Springer-Verlag London Ltd., part of Springer Nature 2019 Abstract This research aims to observe and compare the wound healing process of urethral bladder after transurethral holmium laser resection of bladder tumor (HoLRBT) and transurethral resection of bladder tumor (TURBT) and explore the possible mechanism of wound healing and bladder re-epithelialization after HoLRBT. An animal model of canine achieving HoLRBT and TURBT was established. Cystoscopy was performed at different time points (3 days and 1, 2, 3, and 4 weeks) after operation to observe the wound healing and re-epithelialization of bladder epithelium. Bladder mucosa specimens were obtained and histopathological changes of the bladder epithelium were observed under light microscope after HE staining. Immunochemistry was used to determine the cell expression ofCK5, CK14, EGF, EGFR; microRNA expressions of CK5, CK14, EGF, and EGFR were measured by qRT-PCR. The changes of urinary EGF concentration were detected by ELISA. The bladder epithelial wound was repaired and re-epithelialized at 1 week after HoLRBT. At the 4th week, the bladder wound was basically completed and re-epithelialized; repair of bladder epithelial wounds recapitulates the wounds with the proliferation and migration of residual epithelial cells under the wound and the bladder epithelium that proliferates alongside the wound surface to complete re-epithelialization. The process begins at 1 week after surgery and basically completes at 4 weeks after surgery. CK5 and CK14 positive cells were detected in the basal cells of the bladder epithelium after HoLRBT, and the expression of CK5 and CK14 mRNA in the basal cells of the bladder epithelium under hyperplasia was significantly higher than that of the normal bladder epithelial basal cells. Bladder epithelial wound repair of TURBT group was performed by the proliferative differentiation of the peri-bladder epithelium adjacent to the wound edge and crawled to the wound surface to complete the re-epithelialization process. The wound repair and re-epithelialization were significantly slower than HoLRBT group. The CK5 and CK14 positive cells can also be detected in the basal cells of marginal hyperplasia of basal margin, and the expression of CK5 and CK14 mRNA in the basal cells of the peri-bladder hyperplasia is obviously higher than that of the normal bladder epithelial basal cells. The expression of EGF in bladder regenerating epithelium gradually increased with time after HoLRBT. Bladder basal cells and bladder regenerating epi- thelium express high levels of EGFR after HoLRBT. The concentration of EGF in urine after HoLRBT and TURBT increased significantly after surgery, and peaked at 3 days after operation. The urinary EGF concentration in HoLRBT group was higher than that in TURBT group at 3 and 4 weeks after operation. The re-epithelialization process can be seen 1 week after the cystectomy with holmium laser cystectomy, and the epithelialization rate is faster than the traditional transection surgery. This is because the residual bladder epithelial stem cells and wound marginal epithelial cells are Sha Han, Kai Dong and Mengjun Shen contributed equally to this work. * Wei Zhao 3 Nanjing Medical University, Nanjing 210000, China [email protected] * Dongliang Xu 4 Department of Urology, Shanghai General Hospital, School of [email protected] Medicine, Shanghai Jiao Tong University, 100 Haining Rd, Hongkou District, Shanghai 200080, China 1 Department of Andrology and Urology, Changzhou TCM Hospital, Changzhou 213000, Jiangsu Province, China 5 Department of Urology, Changzheng Hospital, Second Military 2 Department of Urology, Shanghai General Hospital, Shanghai Jiao Medical University, 415 Fengyang Rd, Huangpu District, Tong University School of Medicine, Shanghai 200080, China Shanghai 200003, China 1218 Lasers Med Sci (2019) 34:1217–1227 involved in the process of wound repair and re-epithelialization following HoLRBT. But only the marginal epithelial tissue participates in the re-epithelialization process after TURBT, so the repair rate of TURBT is slower. The repair of bladder epithelium after HoLRBT is related to the stimulation of tissue factor EGF. The regenerated bladder epithelium also participates in the wound repair process by means of autocrine of EGF. Keywords Bladderepithelial stem cells . Wound repair . HoLRBT Bladder cancer was the ninth most common malignancy prostatic urethra after transurethral holmium laser surgery, it worldwide [1]. On average, it is 3 to 4 times more common was found that the re-epithelialization of the prostatic urethra in men than in women [2]. Among the newly diagnosed blad- after surgery was due to residual prostate ducts and acinar der malignancies, non-muscle-invasive bladder cancer epithelial cells under the wound [13]. The process of re- (NMIBC) accounts for 70%, of which Ta accounts for 70%, epithelialization of the prostate is also closely related to the T1 accounts for 20%, and Tis accounts for 10%. At present, stimulation of EGF [14]. However, the contrastive observation the standard treatment of non-muscle-invasive bladder cancer and mechanism study of the repair of bladder mucosal injury is transurethral resection of bladder tumors known as TURBT. after HoLRBT and TURBT has been rarely reported. We hy- Since Parson et al. [3] used laser technology in the urinary pothesize that the wound repair after HoLRBT is also related system for the first time, its advantages of safety and less to the differentiation and proliferation of bladder stem cells in bleeding are rapidly reflected and widely recognized. Laser the basal cells of the urinary bladder, and has an important technology has been popularized in the clinical practice of relationship with the secretion of tissue factor EGF. In this urology [4, 5]. Transurethral resection of the bladder tumor study, a canine transurethral holmium laser/electroresection (HoLRBT) has been widely performed in the treatment of bladder model was established to observe the healing process NMIBC. The prognosis and operation time of HoLRBT and of cystoscopic wounds at various time points after operation TURBT are similar [6]. However, HoLRBT was superior to and its mechanism was preliminary discussed. TURBT in terms of indwelling catheter time, hospital stay, bladder perforation, and obturator nerve reflex rate and inci- dence of postoperative bladder irritation [7, 8]. Although Materials and methods HoLRBT has obvious advantages compared with TURBT, it still cannot completely solve the problem of high recurrence Canines and rapid progression of postoperative tumors. Postoperative bladder infusion chemotherapy can significantly reduce the Thirty male beagle dogs, aged 2, weighing 13–17 kg, were recurrence of non-muscle invasive bladder cancer and is an randomly distributed into two group: a TURBT group and a important treatment after transurethral surgical procedure for HoRBT group. The dogs were adaptively fed with tap water NMIBC [9]. However, the side effect caused by chemothera- and two meals per day for 2 weeks at the Animal Experiment peutic agents such as frequent and urgent urination and urge Center of Shanghai General Hospital, Jiaotong University, urinary incontinence are still of high incidence. The compli- Shanghai. Approval for the animal studies was obtained from cations of infusion chemotherapy seriously affect the quality the Medical Science Ethics Committee of Shanghai General of life and treatment of patients. Compliance has led to the Hospital. occasional pause or termination of intravesical instillation che- motherapy, which has ultimately contributed to the recurrence Modeling of two-micron laser resection of bladder cancer [9]. In order to reduce the side effects of infusion chemotherapy, it usually takes 2–4 weeks after All operations were performed using the same two-micron TURBT to promote better repair and re-epithelization of blad- continuous wave Tm:YAG laser system (RevoLix; Lisa der mucosa [10]. Therefore, the understanding of the process Laser Products, Katlenburg, Germany). The laser wavelength and mechanism of bladder re-epithelialization after HoLRBT was 2.013 μm and the energy was transmitted at 40 W of and TURBT has important clinically applicable value and power output through a flexible 550-μm-diameter fiber. significance for achieving the fastest clinical wound healing After general anesthesia had been achieved with 10% chloral and reducing the complications of bladder instillation. In re- hydrate (0.003 ml g−1), the canine was placed in the supine cent years, it has been found that bladder epithelial stem cells position on the operating table. The lower abdomen was en- are mainly present in CK5+/CK14+basal cells. These stem tered through a medial and longitudinal incision, and the an- cells can self-regenerate and can differentiate and proliferate terior wall of the bladder was freed. A purse suture was per- to form intermediate cells, thereby further generating superfi- formed in the anterior wall the bladder, an incision was made cial cells [11, 12]. In the study of re-epithelialization of the within the purse
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