Has the COVID-19 Pandemic Affected Community-Acquired Urinary Tract Infections in Children? Abdullah Gul1, Ozgur Ekici2*, Salim Zengin1, Caglar Boyaci1 Purpose: To evaluate whether there were any changes in the rates of urinary tract infection (UTI) and antibiotic resistance in pediatric patients during the pandemic period. Materials and Methods: Urine culture samples collected due to suspected UTI were searched retrospectively from our hospital database, and the patients with growth in urine culture were identified. They were divided into 2 groups as Group A (before COVID-19, March 11, 2019- March 11, 2020) and Group B (COVID-19 period, March 11, 2020- March 11, 2021). Also, COVID-19 period was divided into 3 subgroups (March 2020– June 2020: first epidemic peak, July 2020 – November 2020: normalization process, December 2020– March 2021: second epi- demic peak). We adjusted the patient age as <1, 1-6 and 7-18 years. Age, gender, microorganism strain types, and their antibiotic resistance patterns were compared between the 2 groups Results: This cross-sectional study included 250 eligible patients (Group A, n=182 and Group B, n=68) with a mean age of 10.91 ± 5.58 years. The male/female ratio was higher in Group B than in Group A (p = .004). Inci- dence of UTIs was lower in the curfew and restriction periods due to epidemic peaks than normalization process (p = .001). The proportion of E.coli decreased from 80.2% to 61.8% during the pandemic period when compared to pre-pandemic period (p = .001). Group B had lower rates of resistance to ampicillin, fosfomycin and nitrofurantoin for E.coli than Group A (p = .001, p = .012 and p = .001, respectively). Also, Group B had higher rate of uncommon microorganisms and lower rate of resistance to nitrofurantoin for E.coli than Group A in patients aged 7-18 years (p = .003 and p = .023, respectively). Conclusion: Our study demonstrates that the ongoing COVID-19 pandemic process has caused alterations in community-acquired UTIs in children. More hygienic lifestyle may be considered as the main factor in this change. Keywords: coronavirus; covid-19; pediatrics; urinary tract infection INTRODUCTION The urinary tract infection (UTI) is the most com-mon bacterial infection in children(1). Escherichia coli (E. coli) is the most common type of the produced species(1). Early diagnosis and treatment of UTIs in children is essential to prevent the development of renal scarring. Severe Acute Respiratory Syndrome Coronavirus 2 (SARS COV-2), a single-stranded RNA virus with pos- itive polarity that caused Coronavirus disease (COV- ID), was discovered for the first time in November 2019 in Wuhan, China. It has influenced all of humanity since that day and has resulted in a complete change in our daily routine. The first coronavirus case in Turkey was reported on March 11, 2020. Following this date, the schools were closed and quarantine practices began. Curfews was also declared for the entire society, last- ing several days or weeks on specific dates, including weekends and holidays. During the pandemic, hospital admissions for non-COV- ID reasons decreased in the pediatric age group, as well as in all age groups(2). Postponing elective procedures in hospitals, closing the polyclinics or reducing the num- ber of those, and patients' avoidance of coming to the 1Department of Urology, University of Health Sciences, Bursa Yuksek Ihtisas Education and Research Hospital, Bursa, 16000, Turkey. 2Department of Urology, Nusaybin State Hospital, Mardin, 47200, Turkey. *Correspondence: Department of Urology, Nusaybin State Hospital, Nusaybin, Mardin, 47200, Turkey. Tel: +90 531 917 45 90, Fax: +90 (482) 415 33 63, E-mail: ekici_1990@hotmail.com. Received February 2022 & Accepted June 2022 hospital are several factors that contribute to a lower rate of hospital admission. Along with a decrease in hospital admissions, there was a decrease in the rate of some diseases transmitted through contact as a result of protective measures such as mask use, social distance considerations, and adherence to hygiene rules. Al- though this decrease has been observed in diseases such as viral upper respiratory tract infections and asthma(3, 4), studies on urinary tract infections have revealed con- tradictory results(5-7). The purpose of this study was to evaluate whether the COVID-19 period affects the rates of community-ac- quired UTI in children, the distribution of causative bacteria, and the resistance of these bacteria. MATERIALS AND METHODS Study Design Ethical approval was granted by the University of Health Sciences, Bursa Yuksek Ihtisas Training and Re- search Hospital Ethics Committee with reference num- ber 2011/KAEK-25 2021/11-19. One year period prior to March 11, 2020, the date of the first COVID-19 case in Turkey, was defined as the pre-COVID-19 period, and the one year period following this date was defined as the post-COVID-19 period. Also, we divided the Urology Journal/Vol 19 No. 5/ September-October 2022/ pp. 386-391. [DOI:10.22037/uj.v19i.7227] PEDIATRIC UROLOGY post-COVID-19 era into 3 periods based on the inter- vals when the restrictions began (March-June 2020), the restrictions partially decreased (July-November 2020) and the second epidemic peak (December 2020-March 2021). Similarly, the pre-COVID-19 period was divid- ed into 3 intervals for comparative analysis. Inclusion and exclusion criteria This cross-sectional study included the patients under the age of 18 who presented to the Urology polyclinic with suspected UTI symptoms and had bacterial growth in their urine cultures for the first time within one-year intervals (March 11, 2019 - March 11, 2020, and March 11, 2020 - March 11, 2021). We divided the patients into 3 groups according to their age: <1, 1-6, and 7-18. The study excluded the patients with vesicoureteral reflux, posterior urethral valves, urolithiasis, bladder bowel dysfunction, urogenital tract abnormalities, im- mune system disorders and uncircumcised boys. Also, all of the cohort evaluated in our study were sexually naive. Evaluation of urine samples After anamnesis and a thorough physical examination, microscopic findings of centrifuged urine samples from suspicious patients were recorded, in order to make a di- agnosis. Urine samples were obtained by transurethral bladder catheter in children who had not been toilet trained. Midstream urine samples were collected from older children. These samples were incubated overnight at 37°C with a standard loop of Blood agar and Mac- Conkey agar media. In catheterization and midstream urine samples, 103-104 CFU/mL growth was consid- ered significant, while leukocytes in spot urine tests with >5 leukocytes in each field in centrifuged urine were considered significant. Antimicrobial susceptibili- ty testing was performed using a panel of antimicrobial agents based on the causative organism in cultures with significant bacteriuria using the disc diffusion method. Until the antibiogram results were available, prophylac- tic empirical antibiotics based on the local susceptibility patterns were prescribed to the patients. Following that, the treatment was scheduled in accordance with the an- tibiogram results. The patients were divided into 2 groups as Group A (be- fore COVID-19, March 11, 2019- March 11, 2020) and Group B (COVID-19 period, March 11, 2020- March 11, 2021). The difference in UTI rates, distribution of bacteria grown in culture, and antibiotic resistance be- tween two groups were analyzed. Statistical Analysis The normal distribution of data was evaluated using the Kolmogorov-Smirnov test and graphical method via Q-Q plot. The data were presented as median, in- terquartile range, number and percentage. Groups were analyzed using the Mann Whitney U test for quantita- tive data and the Chi-square test or Fisher's exact test for categorical data as appropriate. Also, we used logis- tic regression model to identify possible confounding factors. p < 0.05 was considered as statistically signifi- cant. SPSS 21.0 program was used. RESULTS After 49 patients met exclusion criteria were removed from the study, a total of 250 patients (182 in group A and 68 in group B) were evaluated. During the COV- ID-19 period, there was a huge decrease in the num- ber of patients when compared to pre-pandemic period (variation: -62.64%). The mean age of the patients was 10.91 ± 5.58 (range: 6 months - 18 years). The initial characteristics of the patients are presented in Table 1. Of the patients, 225 had cystitis and 25 had pyelone- phritis. Seven patients (5 in Group A and 2 in Group B) with a clinical pyelonephritis and impaired oral in- take were hospitalized. It was comparable between the groups in terms of hospitalization (p = .967). While E.coli (75.2%), Klebsiella pneumoniae (10%), and Proteus mirabilis (4%) were the most commonly isolated bacteria, bacteria such as P. aeroginosa, Ente- rococcus and streptococcus spp. were observed at a rate of 10.8%. The distribution patterns of the bacteria by gender are shown in Table 2. While no significantly difference in median age was observed between the two groups, there was a signifi- cantly increase in the male/female ratio in group B (p= .004). The hospital admission rates for UTI in the first and second epidemic peak periods were higher than in Group A (p = .001). Despite the fact that E.coli was the most commonly isolated microorganism in both groups, it was significantly less isolated in group B than in group A (61.8% vs 80.2%) (p = .001). Ampicillin resistance for E.coli was also found to be statistically lower in group B than in group A (27.9% vs 58.2%) (p = .001). Furthermore, there was significantly less re- sistance to fosfomycin and nitrofurantoin for E.coli in group B (p = .012 and p = .001, respectively) (Table 3). There was no difference in UTI rates between the two groups according to age groups and infection type (p= .515 and p = .925, respectively) (Table 3). In the sub- group analysis of the patients according to age groups in terms of microorganism strain types and antibiotic resistance patterns, there was no difference in the peri- ods including the patients aged <1 and 1-6 years, while a significant increase was observed at the uncommon microorganisms rate in the group aged 7-18 years dur- ing the COVID-19 period (Table 4). In addition, only the rate of nitrofurantoin resistance for E.coli decreased significantly during the COVID period in the same group (p = .023). Patient’ age did not influence the UTI rate according to the regression analysis (95%CI: 0.842- 1.146, OR: 0.988, p = .874) DISCUSSION COVID-19 has increasingly led to radical lifestyle changes all over the world since its breakthrough. Peo- ple have begun to avoid crowded places in order to prevent transmission. Furthermore, as a result of social regulations in which governments play a role, patients' Table 1. Demographic data of the cohorts Data n=250 Age, years 10.91 ± 5.58 Gender, n (%) Female 199 (79.6) Male 51 Urine microscopy, n (%) < 5 HPF 85 (34) >5 HPF 165 Isolatedmicroorganisms, n (%) Escherichia coli 188 (75.2) Klebsiella pneumonia 25 (10) Proteus mirabilis 10 (4) Others 27 (10.8) The effect of COVID-19 on UTI in children- Gul et al Vol 19 No 4 July-August 2022 308 HPF: High power field Vol 19 No 5 September-October 2022 387 non-emergency hospital admissions have been reduced, and home health services have begun to be used more effectively. Both the reduction in hospital admissions and the emphasis on social distance have resulted in a reduction in some diseases for which crowded environ- ments are risk factors(4). In our study, hospital admis- sions due to UTIs in children decreased during this pe- riod, and the gender predominance along with antibiotic resistance patterns changed. There are some studies in the literature evaluating the changes in UTI rates in children during the pandemic. Pines et al. reported in their study that the number of patients admitted to the hospital with UTI diagnosis de- creased by 47% during the pandemic period compared to the pre-COVID-19 period(6). Similarly, according to the results of a study reported from Scotland, the rate of admission to hospital due to UTI in children decreased by 55.3% in 2020 when compared to 2018 and 2019(8). In the study by Wilder et al., a decrease in hospitalizations due to asthma, bronchiolitis, and pneumonia, which are more clearly related to social distance and viruses, was observed in the pediatric patient group during the COV- ID-19 period compared to the pre-COVID-19 period, while hospitalizations rates for cellulite, gastroesoph- ageal reflux, and UTI did not change(7). Similarly, ac- cording to the results of a multicenter study conducted in Japan, the number of children who required hospital- ization due to UTI during the COVID-19 period did not differ significantly from the pre-COVID-19 period(5). Kuitunen et al. found a significant decrease in the inci- dence of cystitis and pyelonephritis, especially in pa- tients aged 1-6 years during the pandemic period(9). In their national study, similar to our study, a significantly decrease was found in the incidence of UTIs during the periods of restriction-due to epidemic peak intervals. In our study, while there was no difference in the incidence of UTI according to age subgroups between the groups, patients aged 7-18 years in COVID-19 period had higher rate of uncommon microorganisms than those in pre-pandemic period. The reason for this difference may be that day-care centers where have worse hygien- ic condition than homes are kept open for day-care aged children whose caregiver parents have to work during the period of restriction in our country, and elementa- E.coli K. pneumoniae P. mirabilis Others Before COVID-19, n (%) Male 16 (6.4) 8 (3.2) 4 (1.6) 1 (0.4) Female 130 (52) 10 (4) 4 (1.6) 9 (3.6) COVID-19 period, n (%) Male 8 (3.2) 1 (0.4) 1 (0.4) 12 (4.8) Female 34 (13.6) 6 (2.4) 1 (0.4) 5 (2) p value 0.166 0.158 0.990 0.002 Table 2. Distribution of the bacteria by gender between the groups Pediatric Urology 309 Variables Group A (n=182) Group B (n=68) p value Age (years) 11 (IQR: 7-16) 12.5 (IQR: 5.25-16.75) 0.558 Age groups, n (%) 0.515 <1 year 3 (1.6) 1 (1.4) 1-6 years 41 (22.6) 20 (29.4) 7-18 years 138 (75.8) 47 (69.2) Infection type, n (%) 0.925 Cystitis 164 (90.1) 61 (89.7) Pyelonephritis 18 7 Infection period, n (%) 0.01 March-June 46 (25.3) 11 (16.1) July- November 79 (43.4) 44 (64.7) December- February 57 (31.3) 13 (19.2) Gender, n (%) 0.004 Male 29 (15.89) 22 (32.35) Female 153 46 Microorganism, n (%) 0.001 E. coli 146 (80.2) 42 (61.8) K. pneumoniae 18 (9.9) 7 (10.3) P. mirabilis 8 (4.4) 2 (2.9) Others 10 (5.5) 17 (25) Antibiotic resistance for E. coli, % Ampicillin 58.2 27.9 0.001 Piperacillin-tazobactam 18.1 22 0.483 Gentamicin 8.8 7.3 0.715 Amikacin 7.1 1.5 0.083 Ceftriaxone 37.3 35.3 0.763 Cefuroxime 42.8 38.2 0.509 Ceftazidime 39.5 38.2 0.849 Ciprofloxacin 17.5 23.5 0.288 Meropenem 1.6 1.4 0.921 Ertapenem 2.7 1.4 0.557 Fosfomycin 11.5 1.4 0.012 Nitrofurantoin 19.7 2.9 0.001 Trimethoprim-sulfamethoxazole 34.1 29.4 0.485 Table 3. Comparison of pre-COVID-19 (Group A) and COVID-19 period (Group B) data The effect of COVID-19 on UTI in children- Gul et al Pediatric Urology 388 ry, middle and high schools interrupt their education. Kruizinga et al. compared the pediatric emergency de- partment admissions between 2016-2019 and 2020(10). A significant decrease in admissions was observed in February 2020 along with the highest decrease in April 2020. However, in the group of non-communicable diseases including UTI in their study, no significant change was observed between the periods. Similar to the results of study mentioned above, we observed sig- nificantly decrease in the incidence of UTI during the first and second epidemic peak periods in our study. Several hypotheses can explain the decrease in the number of pediatric patients diagnosed with UTI. The first reason could be that schools were closed during this period(11). It is a well-known fact that schools and common areas have usually worse hygienic conditions than homes in our country. The second reason might be that more attention was paid to personal hygiene during this period and interpersonal contact was minimized. Although UTI is not classified as a communicable dis- ease, societal outbreaks have been reported(12). Since E.coli is found in normal intestinal flora, hand and food hygiene appear to play a role in contamination. It is known to be transferred between sexual partners and people living in the same household(13). Third, during the pandemic, parents may have preferred to take their children to branch hospitals where only children can be treated, rather than general hospitals where adults are more numerous. According to the study of Goldmann et al., the decrease in the rate of pediatric admissions to the general hospital emergency department during the pandemic period was 70%, while the fall in the rate of admissions to the pediatric hospital emergency depart- ment was determined as 57%(2). Public health measures against COVID-19 are also known to cause a decrease in other infectious diseas- es. According to a study conducted in Taiwan, the in- cidence of Kawasaki disease reduced by 30% in 2020 when compared to 2018(14). However, it was mentioned that this decline, according to the study's authors, may be a result of both the precautions taken and the de- crease in patients' admission to the hospital. During the pandemic period, a new type of phobia, known as "COVID phobia," emerged(15). Lin et al. reported in their study that as a result of this "COVID phobia," the incidence of emergency department admissions due to respiratory tract infections dropped by nearly 50% in Taiwan(16). However, no similar decrease in rates of UTI Table 4. Analysis of microorganism strain types and their antibiotic resistance patterns according to age groups Variables Group A Group B p value The patients aged < 1 year Microorganism, n 0.500 E. coli 2 0 K. pneumoniae 1 0 P. mirabilis 0 0 Others 0 1 The patients aged 1-6 years Microorganism, n 0.175 E. coli 30 10 K. pneumoniae 6 4 P. mirabilis 3 2 Others 2 4 Antibiotic resistance for E. coli, % Ampicillin 63.3 50 0.482 Piperacillin-tazobactam 23.3 40 0.418 Gentamicin 13.3 20 0.629 Amikacin 3.3 10 0.442 Ceftriaxone 53.3 70 0.471 Cefuroxime 53.3 60 0.734 Ceftazidime 50 60 0.721 Ciprofloxacin 20 30 0.665 Meropenem 6.6 0 0.615 Ertapenem 10 0 0.560 Fosfomycin 16.6 0 0.306 Nitrofurantoin 16.6 0 0.306 Trimethoprim-sulfamethoxazole 43.3 30 0.485 The patients aged 7-18 years Microorganism, n 0.003 E. coli 114 32 K. pneumoniae 11 3 P. mirabilis 5 0 Others 8 12 Antibiotic resistance for E. coli, % Ampicillin 50.8 34.4 0.098 Piperacillin-tazobactam 14.9 15.6 0.921 Gentamicin 3.5 6.2 0.612 Amikacin 0.8 0 0.781 Ceftriaxone 31.5 25 0.474 Cefuroxime 39.4 34.4 0.600 Ceftazidime 34.2 31.2 0.754 Ciprofloxacin 18.4 18.7 0.573 Meropenem 0.8 0 0.781 Ertapenem 0.8 0 0.781 Fosfomycin 8.7 3.1 0.457 Nitrofurantoin 14.1 0 0.023 Trimethoprim-sulfamethoxazole 28.9 28.1 0.559 The effect of COVID-19 on UTI in children- Gul et al Vol 19 No 5 September-October 2022 389 was seen. According to the findings of Roongpisuth- ipong et al., there was a change in the pattern of skin diseases during the COVID-19 period(17). Another result of our research was that the male/female ratio in UTI increased throughout the pandemic peri- od. While female patients used public toilets in schools and playgrounds prior to the pandemic, they met these needs at home since schools were closed and social ar- eas were restricted during the pandemic. Considering that anatomical factors are one of the leading causes of UTI in girls, since houses has better hygienic condi- tions, it is reasonable to predict that the reduction rate of UTI in girls would be more compared to boys. This relative decrease might account for the rise in the male/ female ratio for bacterial growth. Another finding was that the rate of E. coli decreased during the pandemic period when compared to other uncommon causative microorganisms. This might be attributed to a rise in the male/female ratio. In the COVID-19 period, male predomination was observed in the other causative mi- croorganism species in our study. Edlin et al. reported in their research, which involved 24,815 pediatric pa- tients, that microorganisms without E. coli were seen at a higher rate in men than in women(18). In our study, the highest antibiotic resistance for E. coli was observed in ampicillin (50%). It was followed by cephalosporins[cefuroxime (41.6%), ceftazidime (39.2%), ceftriaxone (36.8%)] and trimethoprim-sul- famethoxazole (32.8%). According to Edlin et al., the highest resistance rates were seen in ampicillin (45%) and trimethoprim-sulfamethoxazole (24%) in their investigation(18). Another finding of our study is the change in antibiotic resistance patterns during the COVID-19 period. Resistance for E.coli has declined dramatically, particularly to ampicillin, fosfomycin and nitrofurantoin. There may be several reasons for this change. In general, lockdown, restriction or less person- al interaction with the peers might be the main reasons for this situation. As it is known, pathogen resistance in UTI varies according to time as well as geographical and regional location. For example, in their 6-year study on the change of antibiotic resistance, Erol et al. dis- covered that resistance to ampicillin, trimethoprim-sul- famethoxazole and nitrofurantoin increased whereas cephalosporin resistance remained steady(19). Saperston et al. discovered that E.coli resistance to trimethop- rim-sulfamethoxazole, ampicillin, cephalosporins, and ciprofloxacin differed significantly between inpatients and outpatients(20). Another reason could be that antibi- otic use has dropped throughout the pandemic. Unless a bacterial agent superinfected, the Ministry of Health did not recommend routinely antibiotic treatment for COVID-19 patients in Turkey during the COVID-19 period, but only Favipiravir was utilized. Antibiotic use in other countries has fallen dramatically in both inpatient and outpatient groups(21,22). Travel limitations abroad might have reduced the transfer of regional anti- biotic resistance genes during this period(23). According to a study conducted in Belgium, the use of amoxicillin, which is commonly used to treat respiratory tract infec- tions, declined dramatically during the pandemic peri- od, while the use of nitrofurantoin did not change(24). Based on this information, the decrease in ampicillin resistance may be related to a reduction in the use of this antibiotic group in upper respiratory tract infections during the pandemic. It is believed that the drop in other antibiotic resistances is related to a general decrease in antibiotic use(21,22). Although our study reveals that the proportion of UTI in children has decreased and antibiotic resistance pat- terns have changed during the COVID-19 period, but it also has some limitations. First, our study population consisted of relatively small number of patient groups, and the data were analyzed retrospectively. Second, our study population was limited to our region only and consisted of patients who applied to the general urology polyclinic. As the measures taken during the pandem- ic period differ between countries, results of our study cannot be generalized and cannot represent to the all regions of the world. CONCLUSIONS As a result, hospital admission rate for community-ac- quired UTI in the patients aged ≤18 years has decreased substantially during the pandemic period. Furthermore, male predominance and uncommon microorganism species have increased, and antibiotic resistance pat- terns have changed. Therefore, we think that it would be more appropriate for clinicians to manage the dis- ease by taking into account the changes in the distri- bution of microorganism agents under pandemic condi- tions. Further studies with larger sample size are needed to support the findings of our study. SUMMARY The COVID 19 pandemic has led to lifestyle changes all over the world. All these changes have led to chang- es in the incidence of microorganisms. In our study, we showed that there was a decrease in urinary tract infec- tion rates in children, changes in gender predominance and antibiotic resistance during the pandemic period. CONFLICT OF INTEREST The authors declared no conflict of interest. REFERENCES 1. Jacobson SH, Eklof O, Eriksson CG, Lins LE, Tidgren B, Winberg J. Development of hypertension and uraemia after pyelonephritis in childhood: 27 years follow up. BMJ 1989; 299: 703-6. 2. Shaikh N, Craig JC, Rovers MM, et al. Identification of children and adolescents at risk for renal scarring after a first urinary tract infection: a meta-analysis with individual patient data. JAMA Pediatr 2014; 168: 893- 900. 3. Conway PH, Cnaan A, Zaoutis T, Henry BV, Grundmeier RW, Keren R. 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