Sage Journals: Discover world-class research

Abstract

Objective

Hospital management and medical treatment changed during the coronavirus disease 2019 (COVID-19) pandemic. This study investigated the impact of the COVID-19 pandemic on patients with bladder cancer.

Methods

In this multicenter retrospective study, we collected information from the electronic medical records of outpatients who underwent cystoscopy and inpatients with confirmed bladder cancer in three hospitals in Nanjing (two province-level and one county-level hospitals) in 2019 and 2020. Patients’ home addresses, treatment methods, length of stay, and pathology were compared between the periods.

Results

In total, 4048 outpatients and 1242 inpatients were included. The average number of cystoscopies decreased significantly during the lockdown. In province-level hospitals, the number of cystoscopies increased gradually as the pandemic was brought under control but remained lower than that in 2019, whereas the number grew in 2020 in county-level hospitals. The rates of recurrence and radical cystectomy were higher in 2020 than in 2019. No significant difference in the pathological grade was observed. More patients who underwent radical cystectomy were diagnosed with muscle-invasive bladder cancer during the 2020 lockdown.

Conclusion

The pandemic severely affected patients with bladder cancer, mainly in their choice of institution and treatment.

Keywords

Bladder cancer real-world COVID-19 management recurrence radical cystectomy cystoscopy

Introduction

The outbreak of the coronavirus disease 2019 (COVID-19) pandemic prompted an urgent global response, which included restricted travel, limited patient visits to hospitals, and partly closed operating rooms.¹ The impact of COVID-19 on all aspects of the urology department—a department with a high volume of operations—was unprecedented and included changes to adult and pediatric guidelines in response to the pandemic.^2–4 During the COVID-19 pandemic, the European Association of Urology guidelines recommended that only high-priority and emergency patients be surgically treated and that all procedures be performed by experienced urologists with a minimum amount of staff.⁵

Bladder cancer now ranks ninth among the most common cancers worldwide⁶ and is characterized by a high recurrence rate and rapid progression. Cystoscopy is the gold standard for diagnosing bladder tumors and the best way to screen for recurrence.⁷ According to the depth of tumor invasion, bladder cancer is divided into non-muscle-invasive bladder cancer (NMIBC) and muscle-invasive bladder cancer (MIBC). The prognosis is considerably worse for patients diagnosed with NMIBC who progress to MIBC than those with “primary” MIBC.^8,9 Therefore, timely detection and treatment are vital. However, inexplicably, patients hesitate to see a doctor. For patients with NMIBC, transurethral resection of bladder tumor (TURBT), regular intravesical chemotherapy, and cystoscopic monitoring are the primary treatment options and require frequent hospital visits.⁷ Although radical cystectomy (RC) is the recommended surgical treatment for patients with MIBC, the procedure negatively impacts patients’ quality of life.¹⁰ Although many urological operations were postponed during the pandemic, Stensland et al.¹¹ recommended that surgeons still perform bladder cancer operations such as TURBT for suspected cT1+ bladder tumors, cystectomy for carcinoma in situ refractory to third-line therapy, and cystectomy for MIBC.

It should be noted that the effects of the pandemic have only rarely been reported to date. We analyzed the data from Jiangsu Province Hospital for four equivalent months in 2019 and 2020 and found notable differences in bladder cancer recurrence rates and pathology grades.¹² To further investigate the impact on patients with bladder cancer, we conducted a one-year multicenter retrospective analysis using electronic medical records.

Materials and methods

Study design

In this retrospective study, we collected data from electronic medical records in the urology departments of three hospitals in Nanjing: Jiangsu Province Hospital (Hospital A), a province-level comprehensive Western medicine hospital, Jiangsu Province Hospital of Chinese Medicine (Hospital B), a province-level comprehensive Chinese traditional medicine hospital, and Nanjing Gaochun People's Hospital (Hospital C), a county-level hospital. We further studied outpatients who underwent cystoscopy and inpatients who had been diagnosed with bladder cancer. We defined 23 January 2020—the day the Chinese government announced a lockdown in Wuhan that represented an all-out war on the pandemic—as the start date of the COVID-19 pandemic. We used 30 April 2020 as the mid-point to divide the period between 23 January 2020 and 31 December 2020, when the outbreak was satisfactorily controlled and most schools returned to normal operations. For comparison, we collected data from the same period in 2019, dividing the period into two parts. We collected the following clinical data: patients’ age, sex, home address, initial detection of cancer/recurrence, treatments, pathological grade/stage, time from admission to the first operation, and length of stay.

The reporting of this study conforms to the Strengthening the Reporting of Observational Studies in Epidemiology guidelines.¹³ Because this was a retrospective study in which information was obtained exclusively from electronic medical records, the need for approval was waived by the Ethics Committee of the First Affiliated Hospital of Nanjing Medical University. All patients provided written informed consent.

Participant characteristics

All outpatients who underwent cystoscopy were included, and inpatients with hematuria or suspected bladder tumors were eligible for this study. Inclusion criteria were 1) symptoms of hematuria or bladder mass in imaging examinations; 2) definite bladder cancer; and 3) a first round of chemotherapy or immunotherapy after diagnosis. Exclusion criteria were 1) absence of bladder tumor and 2) two or more rounds of chemotherapy or immunotherapy. The workflow is shown in Figure 1.

Figure 1.

Overview of the workflow.

Statistical analysis

We used an independent-samples t-test to compare measurement data (age, time from admission to first operation, and length of stay) and the χ² test or Fischer exact test to compare count data (sex, home address, initial/recurrence, treatment, pathological grading, and staging). Statistical significance was set at p < 0.05.

Results

Outpatients

A total of 4048 patients (2192 patients in 2019 and 1856 patients in 2020) were included in the study (Table 1). An overall 15.3% decrease in patients was observed in 2020 compared with the equivalent timeframe in 2019. From 1 January to 30 April 2019, 649 patients underwent cystoscopy, whereas only 386 patients (an overall 40.5% decrease) received the examination during the COVID-19 pandemic in the same period in 2020. The results in Hospital A (46.4% decrease) and Hospital B (46.8% decrease) were consistent. However, an 18.6% increase was observed in 2020 in Hospital C, a county-level hospital. The trend is shown in Figure 2. During the 2020 lockdown, the average monthly number of cystoscopies in Hospital A decreased markedly (135.75 ± 23.96 vs. 72.75 ± 31.98, p = 0.020), whereas the number remained consistent in the control period (157.00 ± 11.84 vs. 157.88 ± 15.25, p = 0.900). The opposite trend was observed in Hospital B, which reported a similar number of cystoscopies during the lockdown and a significant decline during the control period. The details of the centers in which patients underwent cystoscopies are shown in Supplementary Tables 1–3.

Table 1.

Data of outpatients who underwent cystoscopy.

	2019 (n = 2192)	2020 (n = 1856)	P value
Sex, n (%)			0.700
Male	1554 (70.9)	1326 (71.4)
Female	638 (29.1)	530 (28.6)
Age, years	62.07 ± 13.69	63.14 ± 13.42	0.013
Number of cystoscopies average month, n
January to April	162.25 ± 29.68	96.50 ± 40.80	0.040
May to December	192.88 ± 14.03	183.75 ± 20.45	0.316
January to December	182.67 ± 24.35	154.67 ± 50.65	0.104
Average number of cystoscopies per week, n
January to April	37.88 ± 10.86	22.12 ± 12.44	<0.001
May to December	44.14 ± 11.66	41.71 ± 11.11	0.375
January to December	42.10 ± 11.68	35.31 ± 14.74	0.011

Figure 2.

The number of outpatients who underwent cystoscopy in 2019 and 2020 in (a) the three hospitals, (b) Hospital A, (c) Hospital B, and (d) Hospital C.

Inpatients

A total of 1440 cases were included. After checking against the inclusion and exclusion criteria, we ultimately accepted 1242 cases (635 cases in 2019 and 607 cases in 2020). Under strict pandemic prevention and control conditions of 2020, the proportion of patients with local recurrence significantly increased (41.4% vs. 30.1%), and more patients received RC (27.0% vs. 18.1%) compared with the same period in 2019. Under the regular pandemic prevention and control period in 2020, the number of patients who received neoadjuvant chemotherapy followed by RC decreased significantly compared with the same period in 2019 (3.7% vs. 17.9%). However, over the entire year, differences were observed only with neoadjuvant chemotherapy (5.0% in 2020 vs. 19.6% in 2019). The annual RC trend is shown in Figure 3. No notable difference was observed in pathologic T staging. Data for inpatients are shown in Tables 2 and 3 and Supplementary Table 4.

Figure 3.

The number of inpatients who underwent radical cystectomy in 2019 and 2020.

Table 2.

Data of inpatients (from January to April).

	2019 (n = 163)	2020 (n = 145)	P value
Sex, n (%)			0.911
Male	129 (79.1)	114 (78.6)
Female	34 (20.9)	31 (21.4)
Age, years	65.83 ± 12.83	65.24 ± 12.08	0.678
Home address, n (%)			0.173
Nanjing	80 (49.1)	60 (41.4)
Outside Nanjing, inside Jiangsu Province	64 (39.3)	58 (40.0)
Outside Jiangsu Province	19 (11.7)	27 (18.6)
Initial /Recurrence, n (%)			0.038
Initial	114 (69.9)	85 (58.6)
Local Recurrence	49 (30.1)	60 (41.4)
Treatment ^a, n (%)			0.067
Conservative ^b	127 (81.9)	100 (73.0)
Radical	28 (18.1)	37 (27.0)
Untreated	8	8
Time from admission to first operation, days	4.85 ± 3.10	5.02 ± 3.05	0.637
Length of stay, days	10.50 ± 7.49	10.98 ± 6.91	0.559
Pathological grade ^c, n (%)			0.121
Low-grade urothelial carcinoma	51 (31.7)	45 (31.5)
High-grade urothelial carcinoma	71 (44.1)	76 (53.1)
Other pathology	39 (24.2)	22 (15.4)
No pathology	2	2
Pathological T staging in RC patients, n (%)			0.948
≤T1	10 (35.7)	14 (37.8)
T2	9 (32.1)	11 (29.7)
T3	7 (25.0)	8 (21.6)
T4	2 (7.1)	4 (10.8)
RC patients who received NAC, n (%)			0.128
No	21 (75.0)	34 (91.9)
Yes	7 (25.0)	3 (8.1)
Admissions in an average month, n	52.33 ± 17.04	46.67 ± 19.60	0.725
Operations in an average month, n	47.67 ± 15.57	43.33 ± 20.50	0.785
Admissions in an average week, n	13.60 ± 3.33	13.29 ± 4.08	0.471
Operations in an average week, n	12.47 ± 2.92	12.41 ± 4.16	0.891

: some of the untreated were excluded from the statistical analysis. ^b: includes transurethral resection of bladder tumor, transurethral laser resection, partial cystectomy, and chemotherapy. ^c: no pathology was excluded from the statistical analysis.

RC, radical cystectomy; NAC, neoadjuvant chemotherapy.

Table 3.

Data of inpatients (from May to December).

	2019 (n = 472)	2020 (n = 462)	P value
Sex, n (%)			0.258
Male	379 (80.3)	357 (77.3)
Female	93 (19.7)	105 (22.7)
Age, years	65.68 ± 12.00	65.36 ± 12.90	0.696
Home address, n (%)			0.356
Nanjing	219 (46.4)	236 (51.1)
Outside Nanjing, inside Jiangsu Province	187 (39.6)	166 (35.9)
Outside Jiangsu Province	66 (14.0)	60 (13.0)
Initial/Recurrence, n (%)			0.475
Initial	335 (71.0)	318 (68.8)
Recurrence	137 (29.0)	144 (31.2)
Treatment ^a, n (%)			0.940
Conservative ^b	362 (81.2)	358 (81.4)
Radical	84 (18.8)	82 (18.6)
Untreated	26	22
Time from admission to first operation, days	5.30 ± 3.77	5.10 ± 3.71	0.414
Length of stay, days	10.53 ± 7.26	9.73 ± 6.92	0.083
Pathological grade^c, n (%)			0.591
Low-grade urothelial carcinoma	141 (3 1.4)	148 (33.3)
High-grade urothelial carcinoma	189 (42.1)	192 (43.1)
Other pathology	119 (26.5)	105 (23.6)
No pathology	23	17
Pathological T staging in RC patients, n (%)			0.203
≤T1	30 (35.7)	23 (28.0)
T2	29 (34.5)	30 (36.6)
T3	23 (27.4)	21 (25.6)
T4	2 (2.4)	8 (9.8)
RC Patients receiving NAC, n (%)			0.003
No	69 (82.1)	79 (96.3)
Yes	15 (17.9)	3 (3.7)
Admissions in an average month, n	59.00 ± 10.10	57.75 ± 8.38	0.792
Operations in an average month, n	54.50 ± 8.82	54.50 ± 8.25	1.000
Admissions in an average week, n	14.50 ± 3.36	14.22 ± 3.67	0.230
Operations in an average week, n	13.52 ± 3.25	13.44 ± 3.50	0.737

: part of the untreated was excluded from statistical analysis. ^b: includes TURBT, transurethral laser resection, partial cystectomy, and chemotherapy. ^c: no pathology was excluded from the statistical analysis.

TURBT, transurethral resection of bladder tumor; RC, radical cystectomy; NAC, neoadjuvant chemotherapy.

In Hospital A, more local recurrences (45.5% vs. 32.3%, p = 0.038) and more RC (28.8% vs. 17.5%, p = 0.043) were observed between January and April 2020 than in the same period in 2019. Evidence of recovery was seen after 1 May 2020, with diagnoses returning to expected levels. In Hospital B, also a province-level hospital, the proportion of patients who underwent RC was higher in January to April 2020 (28.1% vs. 16.7%, p = 0.053) than in the same period in 2019, whereas the recurrence rate was similar. However, in Hospital C, a county-level hospital, no difference was observed in any outcome between the two years. The details regarding inpatients across the various centers are shown in Supplementary Tables 5–13.

Discussion

The COVID-19 pandemic spread rapidly worldwide, forcing unprecedented changes in healthcare systems. To support pandemic prevention and control, outpatients were permitted to visit a hospital only if they had no history of travel to endemic areas and no prior contact with patients who tested positive for COVID-19 in the preceding two weeks.⁵ All hospitalized patients were required to have a negative COVID-19 nucleic acid test, a negative complete blood count, and C reactive protein results within one week and a negative chest computed tomography scan for virus infection within 1 month. The appropriate department was immediately notified and quarantine measures were instituted if a viral infection was suspected.

Cystoscopy is essential for screening and diagnosing bladder cancer. Because of the lockdown, the number of cystoscopic examinations in major hospitals plunged in 2020, resulting in a failure to detect bladder cancer lesions in time and an increased risk of tumor recurrence or progression. Many studies have demonstrated that the fewer invasive tests are performed, the fewer tumors are diagnosed.¹⁴ The declines in colonoscopy and esophagoscopy led to a persistent reduction in the diagnosis and treatment of colorectal cancer^15,16 and esophageal cancer, respectively.² Sud et al.¹⁷ reported that delays in surgery for aggressive cancers increased mortality, observing declines in 5-year survival of more than 17% and 30% with delays of 3 and 6 months, respectively. For example, NMIBC for bladder cancer cannot be delayed by 3 to 6 months, and MIBC can progress after more than 12 weeks of delay from diagnosis or the end of neoadjuvant chemotherapy to RC.^18,19 Strategic prioritization of patients for screening and diagnosis can mitigate progression attributable to delays. Although we observed that more patients were diagnosed with MIBC from May to December 2020 compared with the same period in 2019, the difference was not significant, potentially because we only included patients with RC because of the difficulty cutting down to the muscular layer in patients who underwent TURBT.

The first symptom of bladder cancer is usually hematuria, to which most patients pay little attention, especially during events such as a pandemic. TURBT combined with chemotherapy is the recommended treatment for NMIBC. Subsequently, patients must undergo cystoscopy every 3 months to monitor cancer recurrence. Compared with the same period in 2019, an overall significant increase in recurrences was observed from January to April 2020 and may have resulted from delays in hospital visits. In addition, COVID-19 infection led to delay in intravesical instillations, especially in patients treated with intravesical instillation of Bacillus Calmette–Guerin.²⁰ Interestingly, infusion with Bacillus Calmette–Guerin appears to protect patients from COVID-19 infection²¹ and is worth further exploration. Importantly, however, patients who experience recurrence should monitor traditionally ignored symptoms such as hematuria, which reminds urological surgeons to disseminate scientific knowledge about urological cancers.

In Hospital A, recurrence and RC rates were significantly higher from January to April 2020 compared with the same period in 2019. As one of the most prestigious comprehensive Western medicine hospitals in Jiangsu Province, Hospital A serves many patients with urological cancer; the number of patients with bladder cancer reached 482 and 475 in 2019 and 2020, respectively. However, the number of cancer patients in Nanjing Gaochun People's Hospital remained at a low level (45 patients in 2019 and 43 patients in 2020). The effect of COVID-19 on cancer was modest in county-level hospitals; most cases were common urological diseases such as urinary stones. Because of the specialty of the Chinese medicine center, the number of patients who underwent surgery there was less affected than in the other centers. In summary, hospitals at different levels have differing roles and undertake distinct yet demanding duties.

RC is the primary surgical treatment for MIBC and high-risk NMIBC.^7,10 We observed that more patients chose radical treatment in 2020 than in 2019. Patients must visit the hospital regularly when undergoing conservative treatment such as intravesical chemotherapy, which is inconvenient for patients because of the strict control required. In addition, chemotherapy can lower immunity and increase the risk of pneumonia.²² However, RC has a higher rate of complications and requires that patients repeatedly visit the hospital. A randomized clinical trial that included 302 patients (150 and 152 patients in the robotic and open cystectomy groups, respectively) found that the most common complications of RC were urinary tract infection and postoperative ileus.²³ Bochner et al.²⁴ reported that the rates of grades 2 to 5 perioperative complications were 62% and 66% of the robot-assisted group and open cystectomy groups, respectively. Infectious complications were the most common and required patients to visit the hospital for treatment. Therefore, repeated exposure to medical institutions may also increase the risk of COVID-19 infection. A strategy for patients with bladder cancer who receive alternative therapies is worth exploring.

At the beginning of the COVID-19 pandemic, the number of visits and operations in provincial hospitals collapsed, especially in the first month, by 54.9% and 40.5%, respectively. However, these numbers remained consistent in the county hospital. Surprisingly, an increase in the number of patients who underwent cystoscopy was even observed in 2020. Provincial hospitals, which assumed more responsibility for pandemic prevention and control, were disproportionately affected by the pandemic. Balancing COVID-19 pandemic prevention and the management of patients with cancer requires further study. Boehm et al.²⁵ showed that 84.7% of patients preferred telemedicine during the pandemic, contributing to the further development of telemedicine. Hospital A conducted online consultations from early March 2020. In addition, during the pandemic, patients preferred nearby hospitals, which offered more opportunities for county hospitals. First, pandemic control measures made travel between towns inconvenient for many patients, leading patients to seek medical treatment in local hospitals. Second, avoiding exposure to crowds was a measure to reduce infection risk. Faced with public health emergencies, provincial-level hospitals shouldered the heavy responsibility of controlling the pandemic and county-level hospitals defended the bottom line of basic medical care. Therefore, efforts to enhance comprehensive treatment in county-level hospitals and improve the hierarchical medical system remain crucial. In addition, the application of liquid biopsy for bladder cancer screening is emerging. This rapid and non-invasive strategy may provide more opportunities for patients with bladder cancer.²⁶ Proton imaging could more accurately predict the grade of cancer, providing help for accurate diagnosis.²⁷

Our study had some limitations. First, concerning pathological T staging, we only analyzed the patients who had undergone RC. Second, the number of hospitals in the study was limited. Third, the improvement in the level of treatment level and economic strength may also have an impact on patient visits. Fourth, the data were collected using electronic medical records, which may introduce biases inherent to the retrospective design. More studies are worth exploring to inform how to properly manage patients with cancer during a pandemic.

Conclusion

The COVID-19 pandemic had a severe influence on patients with bladder cancer. Bladder cancer progresses rapidly and should be detected and treated promptly, even during a pandemic. The value of regular surveillance of bladder cancer has been demonstrated. To minimize the risk of virus infection, the concept of a non-invasive bladder cancer examination will be pursued. Sex distribution should also be considered when managing patients during a pandemic. Additionally, advancements in the hierarchical medical system and telemedicine may help provide better care for patients with bladder cancer. Increasing the effectiveness of follow-up and popularizing science for patients with tumors is gradually becoming the surgeon's responsibility.

Footnotes

Author contributions

Conception and design: Qiang Lu, Qingyi Zhu, and Wenhui Qian; data acquisition and analysis: Yong Wei, Hongru Zhu, Juntao Zhuang, Lingkai Cai, Qianying Ji, Peng Chen, and Qiang Cao; and manuscript writing: Yong Wei and Xiao Yang. All authors read and approved the final manuscript.

Data availability statement

All data generated or analyzed during this study are included in this published article and its supplementary information files. Further inquiries can be directed to the corresponding authors.

Declaration of conflicting interests

The authors declare that there is no conflict of interest.

Funding

This research was supported by the National Natural Science Foundation of China (grants No.82072832, 82273152) and the Jiangsu Province Hospital’s (the First Affiliated Hospital of Nanjing Medical University) Clinical Capacity Enhancement Project (JSPH-MC-2021-15).

ORCID iD

Qiang Lu

References

Chan

Yeo

SEK

Chong

, et al. Stepping Forward: Urologists' Efforts During the COVID-19 Outbreak in Singapore. Eur Urol 2020; 78: e38–e39. 2020/03/21. DOI: 10.1016/j.eururo.2020.03.004.

Turkington

Lavery

Donnelly

, et al. The Impact of the COVID-19 Pandemic on Barrett's Esophagus and Esophagogastric Cancer. Gastroenterology 2021; 160: 2169–2171.e1. 2021/01/30. DOI: 10.1053/j.gastro.2021.01.208.

Quaedackers

Stein

Bhatt

, et al. Clinical and surgical consequences of the COVID-19 pandemic for patients with pediatric urological problems: Statement of the EAU guidelines panel for paediatric urology, March 30 2020. J Pediatr Urol 2020; 16: 284–287. 2020/04/16. DOI: 10.1016/j.jpurol.2020.04.007.

Raheem Ali

Ghazwani

Alowidah

, et al. Impact of COVID-19 on endourology surgical practice in Saudi Arabia: A national multicenter study. Asian J Urol 2021; 8: 416–423. DOI: 10.1016/j.ajur.2021.03.006.

Ribal

Cornford

Briganti

, et al. European Association of Urology Guidelines Office Rapid Reaction Group: An Organisation-wide Collaborative Effort to Adapt the European Association of Urology Guidelines Recommendations to the Coronavirus Disease 2019 Era. Eur Urol 2020; 78: 21–28. 2020/05/08. DOI: 10.1016/j.eururo.2020.04.056.

Cumberbatch

MGK

Jubber

Black

, et al. Epidemiology of Bladder Cancer: A Systematic Review and Contemporary Update of Risk Factors in 2018. Eur Urol 2018; 74: 784–795. 2018/10/01. DOI: 10.1016/j.eururo.2018.09.001.

Babjuk

Burger

Comperat

, et al. European Association of Urology Guidelines on Non-muscle-invasive Bladder Cancer (TaT1 and Carcinoma In Situ) - 2019 Update. Eur Urol 2019; 76: 639–657. 2019/08/25. DOI: 10.1016/j.eururo.2019.08.016.

Schrier

Hollander

Van Rhijn

, et al. Prognosis of muscle-invasive bladder cancer: difference between primary and progressive tumours and implications for therapy. Eur Urol 2004; 45: 292–296. 2004/03/24. DOI: 10.1016/j.eururo.2003.10.006.

Moschini

Sharma

Dell'oglio

, et al. Comparing long-term outcomes of primary and progressive carcinoma invading bladder muscle after radical cystectomy. BJU Int 2016; 117: 604–610. 2015/04/09. DOI: 10.1111/bju.13146.

10.

Witjes

Bruins

Cathomas

, et al. European Association of Urology Guidelines on Muscle-invasive and Metastatic Bladder Cancer: Summary of the 2020 Guidelines. Eur Urol 2021; 79: 82–104. 2020/05/04. DOI: 10.1016/j.eururo.2020.03.055.

11.

Stensland

Morgan

Moinzadeh

, et al. Considerations in the Triage of Urologic Surgeries During the COVID-19 Pandemic. Eur Urol 2020; 77: 663–666. DOI: 10.1016/j.eururo.2020.03.027.

12.

Yang

Zhuang

, et al. Effect of Coronavirus Disease 2019 on Patients with Bladder Cancer in China. Urol Int 2021; 105: 726–728. 2021/02/25. DOI: 10.1159/000512895.

13.

Von Elm

Altman

Egger

, et al. The Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) statement: guidelines for reporting observational studies. Epidemiology 2007; 18: 800–804. 2007/12/01. DOI: 10.1097/EDE.0b013e3181577654.

14.

Dinmohamed

Visser

Verhoeven

RHA

, et al. Fewer cancer diagnoses during the COVID-19 epidemic in the Netherlands. Lancet Oncol 2020; 21: 750–751. DOI: 10.1016/s1470-2045(20)30265-5.

15.

De Jonge

Worthington

Van Wifferen

, et al. Impact of the COVID-19 pandemic on faecal immunochemical test-based colorectal cancer screening programmes in Australia, Canada, and the Netherlands: a comparative modelling study. Lancet Gastroenterol Hepatol 2021; 6: 304–314. DOI: 10.1016/s2468-1253(21)00003-0.

16.

Morris

EJA

Goldacre

Spata

, et al. Impact of the COVID-19 pandemic on the detection and management of colorectal cancer in England: a population-based study. Lancet Gastroenterol Hepatol 2021; 6: 199–208. DOI: 10.1016/s2468-1253(21)00005-4.

17.

Sud

Jones

Broggio

, et al. Collateral damage: the impact on outcomes from cancer surgery of the COVID-19 pandemic. Ann Oncol 2020; 31: 1065–1074. DOI: 10.1016/j.annonc.2020.05.009.

18.

Wallis

CJD

Novara

Marandino

, et al. Risks from Deferring Treatment for Genitourinary Cancers: A Collaborative Review to Aid Triage and Management During the COVID-19 Pandemic. Eur Urol 2020; 78: 29–42. 2020/05/18. DOI: 10.1016/j.eururo.2020.04.063.

19.

Gore

Lai

Setodji

, et al. Mortality increases when radical cystectomy is delayed more than 12 weeks: results from a Surveillance, Epidemiology, and End Results-Medicare analysis. Cancer 2009; 115: 988–996. DOI: 10.1002/cncr.24052.

20.

Krajewski

Moschini

Chorbinska

, et al. Delaying BCG immunotherapy onset after transurethral resection of non-muscle-invasive bladder cancer is associated with adverse survival outcomes. World J Urol 2021; 39: 2545–2552. 2020/11/25. DOI: 10.1007/s00345-020-03522-3.

21.

Khansary

Tavilani

Ghasemi

Gender, Bladder Cancer Healthcare and Burden of COVID-19. Cancer Invest 2023; 41: 58–69. 2022/10/26. DOI: 10.1080/07357907.2022.2140351.

22.

Freedman

Sedrak

Bellon

, et al. Weathering the Storm: Managing Older Adults with Breast Cancer Amid COVID-19 and Beyond. J Natl Cancer Inst 2020; 113: 355–359. 2020/05/26. DOI: 10.1093/jnci/djaa079.

23.

Parekh

Reis

Castle

, et al. Robot-assisted radical cystectomy versus open radical cystectomy in patients with bladder cancer (RAZOR): an open-label, randomised, phase 3, non-inferiority trial. Lancet 2018; 391: 2525–2536. DOI: 10.1016/s0140-6736(18)30996-6.

24.

Bochner

Dalbagni

Sjoberg

, et al. Comparing Open Radical Cystectomy and Robot-assisted Laparoscopic Radical Cystectomy: A Randomized Clinical Trial. Eur Urol 2015; 67: 1042–1050. 2014/12/17. DOI: 10.1016/j.eururo.2014.11.043.

25.

Boehm

Ziewers

Brandt

, et al. Telemedicine Online Visits in Urology During the COVID-19 Pandemic-Potential, Risk Factors, and Patients' Perspective. Eur Urol 2020; 78: 16–20. 2020/05/05. DOI: 10.1016/j.eururo.2020.04.055.

26.

Vinnakota

Sharma

, et al. Urinary biomarkers to mitigate diagnostic delay in bladder cancer during the COVID-19 era. Nat Rev Urol 2021; 18: 185–187. 2020/12/19. DOI: 10.1038/s41585-020-00419-z.

27.

Wang

Cai

Huang

, et al. Amide Proton Transfer-weighted MRI in Predicting Histologic Grade of Bladder Cancer. Radiology 2022; 305: 127–134. 2022/06/29. DOI: 10.1148/radiol.211804.

Impact of the COVID-19 pandemic on bladder cancer patients: a multicenter real-world study

Abstract

Objective

Methods

Results

Conclusion

Keywords

Introduction

Materials and methods

Study design

Participant characteristics

Statistical analysis

Results

Outpatients

Inpatients

Discussion

Conclusion

Footnotes

Author contributions

Data availability statement

Declaration of conflicting interests

Funding

ORCID iD

References