Association between Meteorological Factors and Pediatric Urinary Tract Infections in central China: a 6-years retrospective cohort of 2441 children with UTIs

doi:10.21203/rs.3.rs-3380787/v1

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Association between Meteorological Factors and Pediatric Urinary Tract Infections in central China: a 6-years retrospective cohort of 2441 children with UTIs

https://doi.org/10.21203/rs.3.rs-3380787/v1

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Backgrounds: To investigate the association between meteorological factors and common uropathogens in children with urinary tract infections (UTIs) and assesses the potential influence of weather conditions on pediatric UTIs.

Methods: 2411 data from infants and children with UTIs in a children’s hospital from 2016 to 2021 were retrospectively analyzed. A correlation analysis was conducted to investigate the relationship between the monthly detection number of uropathogens and meteorological factors.

Results: Multiple linear stepwise regression analyses showed a positive correlation between monthly average temperature, precipitation volume, sunshine hours, monthly total number of uropathogens, and the number of Escherichia coli and Enterococcus faecalis. Enterococcus faecium was predominant in <12-month-old children, while E. coli was dominant in the 3–18-year age category. E. faecium showed a higher prevalence in girls, while E. faecalis was more prevalent in boys. E. coli exhibited resistance rates of >40% to second- or third-generation cephalosporins in multiple age groups. E. faecium showed high resistance rates to tetracyclines, fluoroquinolones, erythromycin, ampicillin, and penicillin, while Klebsiella pneumoniae displayed higher sensitivity to cephalosporin–sulbactam and sulfamethoxazole, but higher resistance rates to ampicillin, cefazolin and ceftazidime.

Conclusions: This study reveals the association between meteorological factors and uropathogens in children with UTIs, as well as the distribution, age-related characteristics, gender differences and antibiotic resistance profiles of pathogenic bacteria. These findings inform the development of targeted strategies for UTI prevention and treatment based on uropathogenic characteristics and meteorological conditions.

pediatric urinary tract infections

uropathogens

distribution characteristics

meteorological factors

antibiotic resistance

retrospective study

Urinary tract infections (UTIs) are a common infectious disease characterized by the invasion of pathogens into the urinary tract, including the urethra, bladder, and kidneys^[1]. UTIs are common worldwide and pose a significant burden on the health and quality of life of the individual, as well as the economy of countries^[2]. Among the various populations, UTIs in children have attracted widespread attention and research efforts^[3]. UTIs are relatively common in children, particularly in infants and preschool-aged children. The incidence of UTIs in children varies based on age, gender, and population differences. Girls are more susceptible to UTIs than boys, which may be attributed to physiological factors such as a shorter urethra and closer proximity of the urethral opening to the anus in girls^[3]. Additionally, the immature immune system of children contributes to a lower resistance against pathogens, increasing their susceptibility to UTIs^[4].

Understanding the distribution of pathogens, age-related characteristics, and antibiotic resistance is crucial for the management and understanding of pediatric UTIs^[5]. Although previous studies have reported on the prevalence of different pathogens that cause UTIs in children, there is still a lack of a deeper understanding of their age-related characteristics and antibiotic resistance^[6][7]. Furthermore, the relationship between meteorological factors and bacterial infections is attracting an increasing research interest^[8]. Meteorological factors such as temperature, humidity, and sunlight exposure are believed to influence the growth, survival, and transmission of bacteria, thereby affecting the incidence and severity of infectious diseases^[9]. Previous studies have explored the impact of meteorological conditions on UTIs incidence^{[10, 11]}. However, many of these studies were limited to adult populations. Additionally, there is a lack of research on the correlation between specific pathogens causing UTIs and meteorological factors. Our study fills this gap by investigating the correlation between meteorological factors and pathogenic bacterial infections in pediatric UTIs, building upon a comprehensive understanding of the distribution of pathogens, age-related characteristics, and antibiotic resistance.

By studying patients of different ages and genders, we aim to gain further insights into the distribution and characteristics of pathogens in these specific populations, providing more accurate evidence that would enable individualized treatment and management.Additionally, through this research, we aim to uncover the prevalence of pediatric UTIs and their potential relationship with climatic factors, providing a deeper theoretical foundation and clinical guidance for the prevention and treatment of pediatric UTIs.

2.1. Study population

From 2016 to 2021, 30,553 urine culture samples were collected from pediatric patients at a children’s hospital in central China (Fig. 1). However, we excluded 28,076 culture-negative samples and 46 isolates from our analysis because of multiple culture results from the same patient during hospitalization, or contamination indicated by the presence of more than three isolates of organism. For this study, a UTIs was defined as a urine culture showing a growth of 10⁵ CFUs/mL of one or two organisms in the midstream urine specimen, 10⁴ CFUs/mL in the catheter urine specimen, or 10³ CFUs/mL in the percutaneous nephrostomy (PCN) or suprapubic urine specimen, following the latest guidelines provided by the European Association of Urology/European Society for Pediatric Urology^[12]. The remaining unclassified urine cultures, including those with no growth, were categorized as UTIs-negative. To explore the potential association between meteorological factors and specific pathogens causing UTIs, we narrowed down our study population to pediatric UTIs caused by a single pathogen species (N = 2411). The study protocol was approved by the Ethics Review Committee of Wuhan Children's Hospital.

2.2. Strain identification and antibiotic susceptibility tests

The isolates were identified using matrix-assisted laser desorption ionization-time of flight mass spectrometry (MALDI-TOF MS; Bruker, Germany). Antibiotic susceptibility tests were performed using the VITEK 2 automated system (bioMérieux, France) in accordance with the guidelines of the Clinical and Laboratory Standards Institute (CLSI). Quality control strains, including Escherichia coli ATCC 25922, Staphylococcus aureus ATCC 25923, and Pseudomonas aeruginosa ATCC 27853, were used.

2.3. Data on meteorological factors

Data on monthly meteorological factors from 2016 to 2021 were obtained from the publicly accessible China National Meteorological data sharing system. Meteorological factor variables, such as average temperature (°C), relative humidity (%), average volume of precipitation (mm), and sunlight hours (h), were used.

2.4. Statistical analysis

Statistical analysis was performed using SPSS 24.0 software. Categorical variables were analyzed by χ²-test or Fisher’s exact test. OriginLab version 2021 (OriginLab Corporation, Northampton, MA, USA) was used to perform the analyses and draw the figures (pathogen distribution diagram and antimicrobial resistance rates figures). Multiple linear stepwise regression analysis was conducted to explore the relationships between the monthly detection of major uropathogens and meteorological factors. A significance level of p ≤ 0.05 was considered statistically significant.

3.1 Distribution of the main uropathogens

A total of 30,553 urine samples were analyzed. Note that 2,411 strains of pathogenic bacteria were isolated from all midstream urine samples, resulting in a positive rate of 7.9%, with the following yearly distribution: 677 in 2016, 481 in 2017, 365 in 2018, 291 in 2019, 282 in 2020, and 315 in 2021. The age group of 29 days to 6 months exhibited the highest positive detection rate, while no significant difference was observed in the positive rates between different genders (Supplementary Table 1).

Among all the positive results, Gram-negative bacteria accounted for 50.5% (1217), Gram-positive bacteria for 48.0% (1157), and fungi for 1.5% (37) of the isolated strains. The top 10 pathogenic bacteria were E. coli (27.1%), Enterococcus faecium (24.6%), Enterococcus faecalis (20.7%), Klebsiella pneumoniae (8.7%), Pseudomonas aeruginosa (2.8%), Enterobacter cloacae (2.1%), Klebsiella oxytoca (1.8%), Klebsiella aerogenes (1.5%), Proteus mirabilis (1.4%), and Morganella morganii (1.2%). Among the Gram-positive bacteria, E. faecium showed a significant increase in the detection rate, from 15.4% in 2016 to 28.3% in 2021. E. faecalis also exhibited some fluctuations, although it maintained a consistent detection rate, reaching 26.7% in 2021. In contrast, Gram-negative bacteria, such as E. coli, demonstrated a gradual decline in the detection rate, decreasing from 31.6% in 2016 to 21.9% in 2021. K. pneumoniae, another common Gram-negative species, remained relatively stable with a detection rate of 5.1% in 2021. Other bacteria, including P. aeruginosa, E. cloacae, and K. oxytoca, showed varying detection rates without significant overall trends (Supplementary Table 2).

3.2 Age distribution prevalence characteristics of the main uropathogens

Figure 2 presents the comprehensive etiological distribution across various age groups. E. faecium was predominant in the neonatal group (50.9%, N = 58), the 29-day–6-month group (26.0%, N = 208), and the 6–12-month group (33.8%, N = 138). Conversely, E. coli was the dominant pathogen in the 3–6-year age category (33.5%, N = 110) and the 6–18-year age category (36.8%, N = 123).

3.3 Distribution of main uropathogens in relation to gender

Supplementary Table 3 presents the distribution of the main uropathogens in relation to gender. The prevalence of E. coli was similar between girls (27.8%) and boys (26.5%) (p = 0.452). However, significant gender differences were observed for other pathogens. E. faecium showed a higher prevalence in girls (31.8%) compared to that in boys (17.1%) (p < 0.01). In contrast, E. faecalis was more prevalent in boys (23.1%) than it was in girls (18.4%) (p < 0.05). K. aerogenes, P. mirabilis, and M. morganii were also found to have significantly higher prevalence in boys than they had in girls (p < 0.05). However, no significant gender differences were observed for K. pneumoniae, P. aeruginosa, E. cloacae, and K. oxytoca.

The etiological profile of boys and girls of different age groups is shown in Supplementary Table 4. The prevalence of E. coli exhibited an increasing trend in girls with advancing age, while it remained stable in boys. Notably, E. faecium was the predominant pathogen in newborns of both genders, accounting for 46.3% of cases in boys and 55% in girls (Supplementary Table 4).

3.4 Correlation between monthly detection of the main uropathogens and monthly mean values of meteorological factors

Considering the correlation between various meteorological factors (co-linearity), multiple linear stepwise regression analysis was conducted with the total number of pathogenic bacteria detected per month and five main pathogens (E. coli, E. faecium, E. faecalis, K. pneumoniae, and P. aeruginosa) as dependent variables and monthly sunshine hours, average temperature, relative humidity, and precipitation volume as independent variables. Furthermore, considering the potential impact of seasons on the results, we simultaneously included the seasonal factor as an independent variable in the regression analysis (Supplementary Table 5).

The total number of pathogenic bacteria was found to be significantly correlated with the monthly average temperature (p < 0.05, adjusted R² = 0.114) (Supplementary Table 5, Fig. 3a). Specifically, the detection of E. coli showed significant correlations with both the precipitation volume (mm) and sunshine hours (h). Increased precipitation was associated with a higher detection of E. coli (standardized coefficient = 0.281, p = 0.015), suggesting a potential link between rainfall and bacterial contamination. Additionally, more sunshine hours were positively correlated with E. coli detection (standardized coefficient = 0.24, p = 0.037). Detection of E. faecalis also exhibited a significant correlation with the volume of precipitation (mm) (standardized coefficient = 0.387, p = 0.001) (Supplementary Table 5, Fig. 3b and 3c).

3.5 Resistance of the main uropathogens to common antibiotics

E. coli, E. faecium, E. faecalis, and K. pneumoniae were the top four species detected in all age categories. Their antibiotic resistance rates based on different age categories are shown in Figs. 5–8. The resistance rates of E. coli to amoxicillin–clavulanic acid, piperacillin–tazobactam, tobramycin, amikacin, and nitrofurantoin were low in all age categories, while that to ampicillin–sulbactam was lower in the ≤ 28-day age group than that in other age groups. Similarly, E. coli exhibited lower resistance rates to chloramphenicol and gentamicin in the 29-day–6-month age group. In contrast, the 1–3-year age group showed elevated resistance rates for cefotaxime (76.2%), ceftazidime (66.7%), cefepime (69.2%), and aztreonam (67.8%). In general, the resistance rates of E. coli against second- or third-generation cephalosporins were consistently high (surpassing 40%) across all age categories (Fig. 4a).

E. faecium exhibited no resistance to linezolid, vancomycin, tigecycline, and furazolidone across all age groups. Among the tested antibiotics, E. faecium demonstrated relatively lower resistance rates to high-level gentamicin in the 29-d–6-month and 6–12-month age groups, with 13.6% and 13.4% rates, respectively. Conversely, a higher resistance to nitrofurantoin was observed in the 6–18-year age group, while the resistance to fosfomycin increased in the 3–6-year age group. Notably, E. faecium displayed comparatively higher resistance rates to tetracycline, fluoroquinolones, erythromycin, ampicillin, and penicillin (Fig. 4b).

E. faecalis did not demonstrate any resistance to linezolid, vancomycin, tigecycline, and furazolidone across all age categories. Relatively low resistance levels to fosfomycin, penicillin G, and nitrofurantoin were observed in most age groups, except for the ≤ 28-day group. Notably, high resistance rates against fluoroquinolones were observed in both the ≤ 28-day and 6–18-year age groups (Fig. 5a).

Cefoperazone–sulbactam and fosfomycin demonstrated remarkable effectiveness against K. pneumoniae, as they showed 100% sensitivity across all age categories. High resistance rates to ampicillin, ampicillin–sulbactam, and cefazolin, ranging from 35.7–100%, were observed in all age groups. K. pneumoniae exhibited lower resistance rates to the aminoglycoside antibiotics, including amikacin, gentamicin, and tobramycin, in the 3–6-year and 6–18-year age groups. Conversely, higher resistance rates against third-generation cephalosporins, such as cefotaxime and ceftazidime, were observed in several age groups, including 49.5% and 51.6% in the 29-d–6-month age group, 55.6% and 56.2% in the 1–3-year age group, and 38.9% and 45.5% in the 3–6-year age group (Fig. 5b).

UTIs are the most common bacterial infections in children. However, their clinical presentation can vary significantly^[13]. The use of urine culture is still considered the gold standard for the diagnosis of UTIs^[14]. This research is the first large epidemiological study to systematically investigate the association between meteorological factors and the pathogens causing UTIs in a 6-years retrospective cohort of 2441 pediatric patients with UTIs. Our findings reveal interesting results through multiple linear stepwise regression models, indicating positive correlations between the total number of pathogenic bacteria (especially, E. coli, and E. faecalis) causing UTIs and the average monthly temperature, precipitation, and hours of sunshine.

Our study reveals that temperature affects the occurrence of UTIs in children. The significant correlation between the total number of pathogenic bacteria and the monthly average temperature suggests that warmer weather may contribute to the proliferation and survival of these bacteria. Dehydration due to warmer weather leading to lower urine output has been proposed as a possible reason for the seasonality of UTIs^[15–17].

Furthermore, warmer weather may have other effects that increase the risk of UTIs. For instance, bacterial burden near the urethral opening tends to increase during warmer weather^[10], as does bacterial skin colonization^[18]. The positive correlation between the UTIs caused by E. coli and E. faecalis with precipitation can be attributed to several factors. Increased precipitation can lead to higher concentrations of E. coli in urban streams and may wash fecal matter into storm drains and environmental water^{[19, 20]}, thereby increasing children’s exposure and risk of developing UTIs.

The positive correlation between the E. coli detection count in the urinary tract and sunshine hours may be attributed to the extended outdoor activity time for children during longer daylight periods. Additionally, in China, the common practice of using diapers for children could potentially contribute to this correlation. Increased sunshine hours may result in more frequent and prolonged diaper usage, creating favorable conditions for the proliferation of E. coli and potentially increasing the risk of UTIs. However, further research is needed to validate these hypotheses and establish a direct causal relationship.

The climate in Wuhan is known for its scorching heat, earning it the nickname “furnace.” This is especially true during the months of May to July when the city experiences intense summer heatwaves. Consequently, there is a likelihood of increased usage of recreational water facilities such as swimming pools and water sprays. Children have a preference for water play, which undoubtedly raises the risk of UTIs.

Our study demonstrated E. coli as the main causative agent of UTIs among the children of Wuhan (27.1%), followed by E. faecalis (24.6%) and E. faecalis (20.7%). Other studies have indicated E. coli, K. pneumoniae, and P. aeruginosa to be major pathogens^[21–23]. These discrepancies in study findings may be attributed to regional variations, differences in environmental factors, and variations in population demographics. Our findings also revealed interesting patterns regarding the predominance of specific pathogens in different age groups and gender differences in pathogen distribution. Children aged 0–1 year were the major demographics at risk of infection by E. faecium, while those aged 3–18 years were the major demographics at risk of infection by E. coli. Significant gender variations were also noted. E. faecium exhibited a higher prevalence in girls than it did in boys, while E. faecalis showed a higher prevalence in boys. Similar gender disparities were observed for K. aerogenes, P. mirabilis, and M. morganii. These findings suggest that the distribution of certain pathogens may be influenced by gender-specific factors^[24]. Furthermore, the etiological profile of E. coli demonstrated an increasing trend in girls with advancing age, while it remained stable in boys. Additionally, both male and female newborns were predominantly affected by E. faecium, indicating its significance as a common pathogen in the early stages of life^[25].

In addition, our study demonstrated that resistance rates to ampicillin, sulfamethoxazole–trimethoprim, penicillin, tetracycline, fluoroquinolones, and cephalosporins were higher in all age groups. These findings suggest that the inappropriate use of these drugs, particularly in community settings, may contribute to the observed elevated resistance rates. However, it is noteworthy that E. coli demonstrated resistance rates of < 10% against carbapenems, piperacillin–tazobactam, and nitrofurantoin. Therefore, these antibiotics could be considered as suitable empirical treatment options for UTIs caused by E. coli. Additionally, E. faecium and E. faecalis showed no resistance to linezolid, vancomycin, tigecycline, and furazolidone across all age groups. Hence, these antibiotics are effective treatment options.

Resistance patterns may vary across different age groups, For example, E. faecium showed relatively lower resistance to high-level gentamicin in the 29-d–12-month age groups. E. faecalis exhibited high resistance rates to fluoroquinolones in both the ≤ 28-day and 6–18-year age groups. Therefore, it is important to consider the age group when selecting appropriate treatment options for enterococcal infections.

The novelty of this study lies in integrating the distribution of pathogens, age-related characteristics, antibiotic resistance, and the correlation with meteorological factors, providing a comprehensive understanding of uropathogenic infections in pediatric UTIs and their association with meteorological factors. This will contribute to a better understanding of the pathogenesis of pediatric UTIs and provide a scientific basis for developing more effective prevention and treatment strategies. Moreover, this study will provide valuable clinical guidance to pediatricians. By understanding the distribution of pathogens and antibiotic resistance in different age groups of children with UTIs, healthcare professionals can make better-informed decisions regarding appropriate antibiotic treatment and avoid the issues of antibiotic resistance resulting from overuse. Furthermore, investigating the association between meteorological factors and pediatric UTIs can help predict and address seasonal peaks and develop relevant preventive measures.

Our study has several limitations. First, the study was conducted in a single healthcare facility with pediatric patients mainly from Wuhan. Hence, we cannot generalize our findings to other populations or districts. Hence, future studies should consider multicenter and/or multipopulation-based approaches. Second, the study focused on the association between meteorological factors and the prevalence of pathogenic bacteria. However, it did not explore the underlying mechanisms or causality. Therefore, further research is needed to elucidate the specific pathways through which weather conditions may influence the occurrence and spread of pediatric UTIs. Additionally, changes in pathogen distribution and antibiotic resistance patterns over time were not extensively explored. Longitudinal studies with extended follow-up periods would be valuable in monitoring temporal trends and assessing the effectiveness of interventions aimed at mitigating antibiotic resistance in pediatric UTIs.

Despite these limitations, our results still fills the gap between meteorological factors and pathogenic bacterial infections in pediatric UTIs,and provide valuable insights into the potential impact of meteorological factors on pediatric UTIs, revealing the common pathogens that cause pediatric UTIs.

Our study reveals the association between meteorological factors, such as temperature, humidity, and sunlight exposure, with uropathogens in children with UTIs. We also provide a comprehensive understanding of the distribution, age-related characteristics, gender differences, and antibiotic resistance profiles of pathogenic bacteria causing UTIs in children. By studying patients of different ages and genders, we have gained further insights into the distribution and characteristics of pathogens in these specific populations, providing more accurate evidence that would enable individualized treatment and management. And we also uncovered the prevalence of pediatric UTIs and their potential relationship with climatic factors, providing a deeper theoretical foundation and clinical guidance for the prevention and treatment of pediatric UTIs.

CLSI: Clinical and laboratory standards institute; E. cloacae: Enterobacter cloacae; E. faecalis: Enterococcus faecalis; E. faecium: Enterococcus faecium; K. aerogenes: Klebsiella aerogenes; K. oxytoca: Klebsiella oxytoca; K. pneumoniae: Klebsiella pneumoniae; P. aeruginosa: Pseudomonas aeruginosa; P. mirabilis: Proteus mirabilis; M. morganii: Morganella morganii; UTIs: urinary tract infections

Ethics approval and consent to participate

The study protocol was approved by the Ethics Review Committee of Wuhan Children's Hospital.

Consent for publication

All authors are aware of their being listed as a co-author of the paper and have approved the final manuscript and the submission to the journal.

Availability of data and materials

Not applicable.

Competing interests

All authors declared no conflict of interest existed in this work.

Funding

This study was supported by the National Natural Science Foundation of China (Grant No. 82072351), Wuhan Municipal Health Commission of China for the scientific research project (Grant No. WX20C10, WX20D30) and Wuhan Municipal Health Youth Talent Training Program (2021).

Authors' contributions

Changzhen LI, Feng TANG and Xiaomei WANG designed and conceptualized this study; Ye ZENG, Wanjun LUO and Jianjun LIU collected the initial data and preliminarily analyzed the data; Changzhen LI, Ye ZENG and Xiaomei WANG drew the figures and tables and drafted the initial manuscript; Feng TANG and Wanjun LUO revised this manuscript; All authors have read and approved the final manuscript.

Acknowledgements

Not applicable.

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No competing interests reported.

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Association between Meteorological Factors and Pediatric Urinary Tract Infections in central China: a 6-years retrospective cohort of 2441 children with UTIs

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Abstract

Figures

1. Background

2. Methods

2.1. Study population

2.2. Strain identification and antibiotic susceptibility tests

2.3. Data on meteorological factors

2.4. Statistical analysis

3. Results

3.1 Distribution of the main uropathogens

3.2 Age distribution prevalence characteristics of the main uropathogens

3.3 Distribution of main uropathogens in relation to gender

3.4 Correlation between monthly detection of the main uropathogens and monthly mean values of meteorological factors

3.5 Resistance of the main uropathogens to common antibiotics

4. Discussion

5. Conclusions

Abbreviations

Declarations

References

Additional Declarations

Supplementary Files

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