Introduction

The novel coronavirus 2019 (COVID-19) has been responsible of a new rapidly spreading viral infection classified as pandemic on March 11, 2020 by World Health Organization (WHO) [1].

In July 2020, more than 13,340,000 cases have been registered worldwide including 578,000 deaths. By the end of January 2020, all provinces in mainland of China reported cases of COVID-19. By the beginning of February 2020, 44,672 cases were reported in all 31 provinces of mainland of China, with the peak reached on February 12th, 2020. The Hubei province was the first to report absence of new confirmed cases on March 18th 2020, followed by other 23 provinces. By March 23rd 2020, a total of 81.773 cases were reported in 31 provinces of mainland of China, with 8 provinces with no new cases and vast majority of new diagnoses made on patients coming from abroad [2].

This exponentially growing number of cases, has rapidly overwhelmed Health Care Systems and saturated hospital services across the world, causing a significant disruption of elective and emergency activities. In fact, there has been a dramatic change in clinical priorities, both medical and surgical, with urology services affected in several ways. Non-urgent operations have been postponed, emergency cases were advised to be managed differently, aiming to reduce the number of patients requiring hospitalization and access to operating rooms and intensive care units [3]. Additionally, in many cases, urologists had been redeployed in the emergency services to support the care of COVID-19; elective out-patients clinics were also stopped because of the risk of gathering people within the hospital implementing services of telemedicine [4]. Additionally, due to restrictions and uncertainties related to the pandemic, several patients may have decided to not report to hospital for assistance, with a potential risk of clinical deterioration of their conditions.

Endourological procedures were also dramatically affected, even though urinary stones are considered a benign condition, they can lead to severe complications if not treated timely such as urosepsis, renal function deterioration, prolonged pain, need of repeated access to Emergency Care Services, etc. This may represent a risk for patients and, at the same time, an overload for Health Care Systems struggling already to deliver an adequate care during the outbreak [5]. A delayed treatment may also lead to a poor quality of life for patients with urinary stones, for example because of prolonged stent-related irritative symptoms, anxiety, stone growth requiring a more invasive procedure at a later stage.

In this study, we describe the effect of COVID-19 pandemic on urological procedures for upper urinary tract stones in three highly specialized Chinese Institutions during the first outbreak.

Materials and methods

We conducted a retrospective study involving three tertiary referral high-volume Centers specialized in the treatments of urinary stones. We compared surgical volumes and peri-operative outcomes during three periods: trimester prior to COVID-19 outbreak (period A), during COVID-19 (period B), and after COVID-19 outbreak (period C). All Centers involved in the study were asked to collect clinical, surgical, and peri-operative data of adult patients (> 18-year-old) undergoing elective and emergency surgeries for upper tract urinary stones and completing at least a 3-month follow-up. Lengths of study periods were decided taking in consideration the duration of first COVID-19 outbreak in China. In fact, the government notified it on January 24th 2020, during Chinese New Year celebrations. Period B was, therefore, defined as the time interval between the beginning of restrictions and their release, happened on April 30th, 2020. Surgical activities have been compared to analogue periods prior and after the emergency. Following this principle, period A started on October 1st, 2019, and finished on December 31st, 2019. Period B was from February 1st, 2020, to April 30th, 2020. Period C was from May 1st, 2020, to July 30th, 2020. These three study periods have been also identified as all involved hospitals were subjected to analogue situations and limitations, aiming to obtain uniform data. We decided to exclude cases carried out in January 2020 as this period contained many national holidays with the potential effect of biasing results.

From beginning of period B to date, as per national regulations, patients must have been rigorously screened for COVID-19 before receiving any surgical treatment. If negative, they were admitted to a COVID-19-free department for either elective or urgent surgical treatment. If positive, they would have been admitted to a dedicated ward with specific precautions measurements and only non-deferrable conditions would have been treated.

According to national and local hospital regulations, there were no formal limitations or prioritization rules on which type of surgeries should have been delivered across China during COVID-19 first wave of pandemic and afterward, after confirmation that patients were COVID-19 free. In fact, surgeons were left free to decide which types of conditions had to be treated based on their patient’s conditions. For the same reason, patients with urinary stones may have delayed their access to hospitals due to social distancing measurements and/or fear to report to hospitals.

In this study, we investigated procedures with intention to treat ureteric and renal stones or complications related to their presence, including extracorporeal shock wave Llthotripsy (SWL), ureterolithotripsy (URS), retrograde intra-renal surgery (RIRS), percutaneous nephrolithotomy (PCNL), ureterolithotomy, and pyelolithotomy. Data have been retrospectively extrapolated from hospital electronic databases. PCNLs were defined as “mini” in case of utilization of an equal or smaller than 22 Fr Sheath. Standard PCNL was defined as > 22 Fr sheath. Procedures were further categorized as elective or emergency cases. Post-operative complications were reported at 30 days post-op using Clavien–Dindo classification [6]. Stone free status (SFR) was evaluated at 1–3 month post-op and cutoff for clinically insignificant residual fragments was fixed at 2 mm. Due to the nature of the study, Centers adopted different imaging modalities during follow-ups, including unenhanced CT scan (NCCT), ultrasound scan of the urinary tract (US), and X-ray of kidney–ureter and bladder (KUB). The study has been approved in each Center by respective ethic committees.

Peri-operative data

Patient’s demographic data included sex and age. Age-adjusted Charlson’s Comorbidities Index [7] was utilized to assess and quantify comorbidities.

Stone characteristics included laterality, stone location, cumulative stone diameter (mm), hydronephrosis (none, mild, moderate, severe). Stone complexity has been reported using the Guy’s Stone Score (GSS) [8]. We also reported the number of patients who preliminarily received a ureteric stent or percutaneous nephrostomy insertion.

Peri-operative data included the rate of patients which received a stent insertion at the end of treatment, 30-days complications rates, mean post-operative length of stay (days from completion of treatment to decision to discharge), SFR. In case of persistence of significant fragments, we also collected the subsequent planned treatment strategy.

Usually, after admission, patients receive full assistance from the pre-operative surgical preparation to the final stone treatment. In case of patients requiring immediate renal drainage, a stent/nephrostomy was placed and generally the stone clearance was completed during same admission as soon as the clinical conditions are favorable.

For this reason, procedures have been divided in emergencies if delivered on first day of admission or elective if carried out after more days and adequate pre-operative work-up. Therefore, emergency procedures include cases operated for different reasons at day-1, including deterioration of renal function, hydronephrosis, infectious complications, pain. Due to the characteristics of the electronic database, we could not record separately ureteric stents and percutaneous nephrostomy placements, as happening during same admission episode.

Statistical analysis

Descriptive statistics were obtained reporting means and standard deviations for continuous variables. Frequencies and proportions were used for categorical variables. Continuous variables were compared using the Student t or the Mann–Whitney U test, based on normal or not-normal distribution. Categorical variables were tested with Chi-square test. All tests were two-sided, and significancy was set at p < 0.05. Statistical analyses were performed using SPSS v.24 (IBM SPSS Statistics for Mac, Armonk, NY, IBM Corp).

Results

Surgical volumes

A total of 2,543 procedures have been delivered across three sites, including 2,062 elective cases and 481 emergency cases (Table 1). During period B, we observed a loss of 457 elective cases (−53.3%) and 286 emergency cases (−93.5%). A more modest decrease was noticed also in period C, including 55 elective cases (−6.4%) and 151 emergency cases (−49.3%). These differences resulted statistically significant (p < 0.001). The most significant reduction was due to PCNLs, with mini-PCNLs reduced by 60.8% in period B and 18.29% in period C. Standard PCNLs showed a worst decrease (−95.2% and −89.2% in period B and C, respectively). Among elective cases, we observed a significant increase of retrograde procedures (+ 31.1% for URSs and + 38.1% for RIRSs) during period C. Same effect was not noticed for emergency cases. Open surgeries included a total of eight procedures. During period B, these procedures have not been carried out, ureterolithotomies were reduced in period C (−25%) but pyelolithotomies increased by 75%. In Table 1, we also reported relative variations of different types of surgery during three periods. In Supplementary Table 1, we reported variations of expenses related to stone surgeries. Compared to period A, costs were reduced by 64.8% and 17.1% during period B and C, respectively.

Table 1 Procedures delivered during trimesters, subdivided in elective and urgent and variations of overall surgical volumes
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Patients and stone characteristics

In Tables 2, 3, 4, and 5, most relevant peri-operative data for PCNLs, RIRSs, URSs, and ESWLs, respectively are reported Additional data are reported in Supplementary Table 2. Patients’ complexity did not change during three periods, with CCI having a mean value between 1 and 2 (p = 0.062 for PCNLs, p = 0.851 for RIRSs, p = 0.763 for URSs and p = 0.397 for ESWLs). During period B, we observed a different level of stone complexity compared to period A. For PCNLs, absence or mild hydronephrosis was observed in 53.5% during period A compared to 64.9% in period B and 58.8% in period C (p = 0.04). Regarding RIRSs, none or mild hydronephrosis was noticed in 72.8% of cases during period A, 81.7% in period B, and 78.3% in period C (p = 0.025). Similar trend was noticed also for URSs, showing 62.2% during period A, 66.7% in period B, and 70.4% in period C (p:0.07). ESWLs did not show the same trend with 97.9%, 96.5%, and 95.7% in periods A, B, and C, respectively (p = 0.189).

Table 2 Peri-operative data on PCNLs
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Table 3 Peri-operative data on RIRSs
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Table 4 Peri-operative data on URSs
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Table 5 Peri-operative data on ESWLs
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GSS was also calculated for PCNLs. In this case, data suggest that more complex procedures have been carried out during the pandemic, with GSS 3 and 4 representing 25.6% of cases during period A, 31.2% in period B, and 24.2% in period C (p = 0.01). For PCNL, 68.8% of patients in period A had multiple/staghorn stones, 81.8% in period B, and 75.7% in period C. For RIRS, 52.2% of patients in stage A had multiple/staghorn stones, 68.8% in period B, and 60.7% in period C.

For PCNL, bilateral stones were observed in 5.4% of cases in period A, 13.3% in period B, and 25.4% in period C (p = 0.001). In period A, 6.8% of cases had both kidney and ureteral stones, 17% in period B, and 11.6% in period C (p = 0.001).

For RIRS, bilateral stones were observed in 4.2% of cases in period A, 5.7% in period B, and 25% in period C (p = 0.004). In period A, 5.6% of cases had both kidney and ureteral stones, 18.7% in period B, and 11.3% in period C (p = 0.01).

Regarding ESWLs, after COVID-19 appearance, the proportion of ureteric stones increased significantly, representing 70.1% in period A, 87.9% in period B, and 78% in period C (p = 0.019).

Using stone diameter data, we also found that post-COVID-19 stone burdens changed in stages B and C. For PCNL, the data showed a greater stone burden in stages B and C, 26.8 in stage A, 28.42 in stage B, and 25.2 in stage C (p = 0.009). For RIRS, the data showed a lower stone burden in stages B and C, 17.15 in stage A, 14.5 in stage B, and 13.9 in stage C (p = 0.0001).

The number of patients pre-operatively stented also increased. For PCNLs, the rates of pre-stented patients were 10.4%, 16.8%, and 33.2% for period A, B, and C, respectively (p = 0.01). For RIRSs, rates were 19.8%, 20.3%, and 42.6% (p = 0.001). For URSs, they were 10.3%, 13.6%, and 39.7% (p = 0.001). This difference was not noticed for ESWLs (p = 0.501).

Intra-operative data and follow-ups

SFRs did not show any relevant difference for PCNLs and ESWLs (p = 0.913 and p = 0.578, respectively) while a difference was noticed for RIRSs and URSs (p = 0.048 and p = 0.013, respectively). For RIRS, SFR in stage A was 69.2%, stage B was 80.5%, and stage C was 69.3% (p = 0.048). For URS, SFR in stage A was 90.3%, stage B was 97.1%, and stage C was 84.8% (p = 0.013). Patients requiring ureteric stenting after treatment increased after period A. In fact, for RIRSs, the rates were 84.4%, 93.1%, and 98.2% in period A, B, and C, respectively (p = 0.001). URSs showed analogue trends, with rates of stented patients of 84.1%, 99.2%, and 97.3%, respectively (p = 0.01). For PCNLs, the rate of patients requiring nephrostomy and/or ureteric stent was 84.4%, 93.1%, 98.2%, respectively (p = 0.001). The Clavien–Dindo Score for complications differed only for PCNLs, with 2.4% of patients in stage A having a score of 2, 2.6% in stage B, and 4% in stage C (p = 0.047). Among patients not stone free, the post-operative strategy did not differ between groups for all types of procedures throughout three study periods.

Discussion

COVID-19 pandemic has caused a significant disruption of Health Care Services and its effects are still evident. The main result was the partial or total interruption of routine clinical and surgical activities.

Naspro et al. documented a reduction of urological surgical volumes by 30% within 15 days from the beginning of the outbreak. Same authors reported a total shutdown on March 19th, 2020. This fact was determined by utilization of hospital beds for COVID-19 patients. Additionally, the capacity of delivering urgent urological operations was significantly affected due to the lack of anesthetists, operating rooms, and ventilators, required for critically ill COVID-19 patients [9].

Furthermore, Novara G et al. reported a 55% decrease of urgent consultations in Italy, with a peak of 64% in areas more severely involved by the COVID-19 pandemic [10].

Similar effects were reported by Bin Hamri et al. [11] in Saudi Arabia. Overall, authors observed a decrease of 78% of out-patients clinic appointments (with 90.8% of them delivered as telephone consultations) and 34% of all elective procedures. Additionally, emergency procedures were reduced by 9.3%.

In China, although preventive measurements have been promptly adopted, we observed a significant reduction of surgical and clinical activities. This effect has been caused by different phenomena which, we believe, have been challenging to control and prevent. On one side, clinicians may have decided to carry out only urgent operations and postpone all non-urgent complex procedures. On the other hand, the isolation protocols introduced in different cities may have limited the possibility of seeking medical assistance. Additionally, we cannot properly quantify the psychological stress and fear of citizens, possibly stopping them from reporting to hospitals. The sum of these events is difficult to clearly quantify but, as shown by our data, has likely determined a temporary significant disruption of quality of Health Services which continued partially even after the complete release of restrictions. In fact, we reported a loss of 743 procedures during period B and 206 procedures during period C.

The impact of the inappropriate management of urinary stones can have a dramatic impact on patients’ safety. As reported by Galiabovitch et al. [12], approximately 10% of all surgical deaths are secondary to stones. Also, urinary sepsis are demonstrated to be responsible for 49.5% of all deaths. Same authors revealed how delayed/suboptimal management of infections was responsible of 39% of these events. Postponed access to medical care and adoption of non-ideal treatments are phenomena widely reported during the pandemic. These data underline how deep the effect of COVID-19 on patients with urinary stones could have been.

The real impact of delayed treatments for urolithiasis is difficult to balance but we can expect an increased risk of renal function loss, ureteric strictures, and infectious complications.

In literature, the delayed management of complications secondary to renal obstruction seems to have caused more dangerous events. Before the pandemic, the mean time between onset of symptoms for obstructing urosepsis and the appropriate intervention was a 2–3 days, with an associated positive correlation between a longer time and occurrence of septic shock [13, 14]. Furthermore, Meller et al. [15] were able to show how during COVID-19 pandemic, patients with obstructive pyelonephritis received delayed assistance (mean of 7.8 days versus 4.3 days of the pre-COVID period) and experiencing more severe clinical conditions including SIRS (57% versus 25%), perirenal abscesses (13% versus 0%), and longer hospitalization (mean 7.6 days versus 3.8 days). In this study, the authors attributed the delay of treatment to strict measures adopted in Brazil and the concomitant reluctance of the population to seek hospital assistance.

In our study, we observed a reduction of emergency treatments too, although our data do not demonstrate an increased incidence of life-threatening events. This fact is likely to be attributed to different factors which have limited access to hospitals. We might speculate that many patients preferred to be managed locally or avoid medical care completely, particularly those with less severe urgent conditions (pain, low-degree fever, asymptomatic renal obstruction, etc.).

To the best of our knowledge, this study represents the first report of COVID-19 effects on the treatment of urinary stones in China. In literature, reports on changes of surgical volumes during the outbreak are sparse and not evaluating patient’s complexity and surgical results. In this study, we analyzed surgical volumes in three highly Specialized Centers including also peri-operative data, documenting how COVID-19 affected treatment decisions.

For PCNLs, our data showed that the number of patients pre-operatively stented was higher in period B compared to period A, whereas the number of nephrostomies has reduced. Additionally, during period B, stone complexity seemed to be higher (31.2% of stones resulted to be GSS 3 or 4 compared to 25.6% in period A and 24.2% in period C, p = 0.01).

In period B, we observed varying degrees of hydronephrosis and stone burden compared to period A. We believe that more patients with complex stones in period B reported to hospitals for non-deferrable reasons (pain, infections, etc.), while those who were generally well and with no obvious symptoms preferred to stay at home and delay treatments. Additionally, for safety reasons, surgeons seemed to be more inclined to stents patients before definitive surgery, which greatly reduces the degree of hydronephrosis during period B. Besides, in our opinion, the more complex scenarios lead to an increased incidence of post-operative complications after PCNL. However, all Centers applied treatment plans to avoid complications through rational surgical selection and good surgeon decision-making.

In our opinion, the reduced number of nephrostomies in favor of the utilization of ureteric stents has been determined by different factors. In fact, percutaneous drainages may come along with risks such as bleeding and dislodgements which may lead to a prolonged length of stay. For this reason, we believe that surgeons have favored ureteric stents to minimize this risk.

Additionally, the rate of “non-tubeless” patients increased during period B. In our opinion, this was due to a higher stone complexity and the need of minimizing the risk of post-operative complications and patients’ re-access to hospitals, which would have been particularly problematic especially during period B. Similarly, the longer post-operative hospital stay has been determined by more cautious strategies.

Regarding RIRS/URSs, data show that the stone burden was smaller during period B and C, coupled with an increased rate of post-operative stent placement and a longer post-operative hospital stay. From an overview of all these elements, it appears evident that, during the pandemic, surgeons preferred treating undelayable large and complex stones with PCNLs and offer RIRS/URS for smaller stones with low risk of post-operative complications. It seems also evident that peri-operative strategies varied, favoring solutions which would have guaranteed lower chances of complications and hospital re-admissions. These phenomena may have determined a deviation from standard and ideal clinical practice alongside increased costs. In fact, such a strategy has obvious effects, greatly improving the SFR of RIRS and URS without affecting the SFR of PCNL. Data presented in this document, seem to have some discordant trends if compared to other geographic regions. In fact, Byrne et al. analyzed treatment modalities for ureteric stones in United Kingdom highlighting a reduced number of patients managed with surgical interventions (from 57.2% to 47.5%) and an increased number of ESWL (from 22.7% to 34.1%). Also, adoption of medical expulsive therapy increased (from 17.4% to 25.4%). In our opinion, these differences have been determined by different factors [16]. Certainly, China is categorized by a very vast territory, and with a less diffused health care network. In this scenario, and with less possibilities of routine monitoring, surgeons in China had to guarantee a more certain resolution of the problem during pandemic period, then favoring more invasive strategies.

In the creation of this study, we certainly expected a drastic reduction of surgical volume during pandemic.

However, certain unexpected results emerged. For example, SWL treatments did not increase compared to retrograde surgeries in period B, although they would have required no anesthesia and hospital admissions. The reason is probably multifactorial and determined by specific case characteristics. We believe that the need to clear the stone in a single treatment was favored; therefore, many surgeons did not opt for SWL. Although rigid safety protocols have been introduced to treat COVID-19 positive stone patients, none of three hospitals reported such cases and all procedures have been carried out in patients free from COVID-19. This also represents an unexpected results.

This study has some limitations. Data have been collected retrospectively. In fact, due to the characteristics of electronic databases and the retrospective nature of the study, we cannot extrapolate the reasons for urgent operations. For the same reasons, data on accesses to Accident & Emergency Departments for stones were unavailable and have not been investigated in this document. In this research, all involved Urology Units are centralized tertiary referral Centers and frequently accepting patients after a diagnosis already obtained locally. In patients requiring treatments, preliminary investigations are usually carried out during same admission and appropriate surgical treatment is usually delivered without the patient returning to hospital at a later stage. In this context, it has not been possible evaluating eventual delays in patients’ treatment as a consequence of the pandemic.

Furthermore, we cannot state whether patients acquired COVID-19 as a consequence of the hospitalization; this was determined by the fact that patients were managed with early discharges when possible. We also need considering that patients could have been located in areas very distant from hospitals, and therefore these elements were not available. Additionally, all procedures have been delivered safely. In fact, all indicators of surgical adequacy (SFR, complication rates and need of subsequent auxiliary procedures) remained similar. However, we acknowledge that a bias may be involved in the comparison of SFR as post-operative imaging modalities adopted for follow-up have been rather heterogeneous, including NCCT, ultrasound, and plain X-rays. Finally, we provided an estimation of costs for treatments of urinary stones (Supplementary Table 2). These data have to be considered indicative as they cannot take in consideration cost related to eventual complications, auxiliary procedure, different medical treatments, etc.

Conclusion

COVID-19 caused a significant disruption of endourological services for urinary stones in terms of both surgical volumes and cases complexity. Alongside a reduced number of treated patients, a deviation from the pre-COVID standard practice has been observed. These effects were still evident after the end of the outbreak and the release of government restrictions. Although the effects of these phenomena in the long term are still uncertain and will need further investigation, in our experience endourological procedures can be adequately and safely carried out.