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Epidemiological characteristics and clinical antibiotic resistance analysis of Ureaplasma urealyticum infection among women and children in southwest China

BMC Infectious Diseases volume 24, Article number: 849 (2024) Cite this article

Abstract

Background

The aim of this study was to investigate the epidemiological characteristics and antibiotic resistance patterns of Ureaplasma urealyticum (UU) infection among women and children in southwest China.

Methods

A total of 8,934 specimens, including urogenital swabs and throat swabs were analyzed in this study. All samples were tested using RNA-based Simultaneous Amplification and Testing (SAT) methods. Culture and drug susceptibility tests were performed on UU positive patients.

Results

Among the 8,934 patients, the overall positive rate for UU was 47.92%, with a higher prevalence observed among women of reproductive age and neonates. The majority of UU positive outpatients were women of reproductive age (88.03%), while the majority of UU positive inpatients were neonates (93.99%). Overall, hospitalization rates due to UU infection were significantly higher in neonates than in women. Further analysis among neonatal inpatients revealed a higher incidence of preterm birth and low birth weight in UU positive inpatients (52.75% and 3.65%, respectively) than in UU negative inpatients (44.64% and 2.89%, respectively), especially in very preterm and extremely preterm neonates. Moreover, the incidence rate of bronchopulmonary dysplasia (BPD) among hospitalized neonatal patients was significantly higher in the UU positive group (6.89%) than in the UU negative group (4.18%). The drug susceptibility tests of UU in the neonatology, gynecology and obstetrics departments exhibited consistent sensitivity patterns to antibiotics, with high sensitivity to tetracyclines and macrolides, and low sensitivity to fluoroquinolones. Notably, UU samples collected from the neonatology department exhibited significantly higher sensitivity to azithromycin and erythromycin (93.8% and 92.9%, respectively) than those collected from the gynecology and obstetrics departments.

Conclusions

This study enhances our understanding of the current epidemiological characteristics and antibiotic resistance patterns of UU infection among women and children in southwest China. These findings can aid in the development of more effective intervention, prevention and treatment strategies for UU infection.

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Introduction

Ureaplasma urealyticum (UU) is a member of the Mycoplasmataceae family with a circular double-stranded DNA genome, which is recognized as one of the smallest and simplest self-reproducing microorganisms [1]. UU is commonly found as a commensal organism in genital tract, with detection rates ranging from 40 to 80% in sexually active females [2]. In addition, it is also considered to be an important opportunistic pathogen during pregnancy [3]. Accumulated studies reported that up to 82% of pregnant women exhibit colonization of UU on vaginal mucosal surfaces [4]. Notably, infections with UU can lead to genital tract inflammation, infertility, chorioamnionitis, premature rupture of membranes, and premature delivery [1, 5]. And pregnant women infected with UU can primarily transmit the pathogen to their neonates through vertical mother-to-child transmission, with transmission rates ranging from 18–88% [6]. Previous studies have shown that premature neonates born before 26 weeks gestation had a positive rate of approximately 65% for UU [7]. In contrast to the majority of adults with asymptomatic infections, neonates with UU infection often experience multiple systemic complications, including bronchopulmonary dysplasia (BPD), intraventricular hemorrhage, necrotizing enterocolitis (NEC), and retinopathy of prematurity [8,9,10]. Therefore, a comprehensive understanding of the infection status and characteristics of UU is crucial.

In terms of treatment, the lack of cell walls in UU severely restricts antibiotic options, and effective drugs for UU infection are limited to those that disrupt protein synthesis and DNA replication. Currently, the main therapeutic drugs used in clinical practice include macrolides, fluoroquinolones, and tetracyclines. While fluoroquinolones and tetracyclines have demonstrated efficacy against UU, their use is limited due to their potential teratogenic effects during pregnancy and adverse impact on bone and tooth development in neonates [11]. The most commonly used class of antibiotics for treating UU infection in pregnant woman and neonates are macrolides, including erythromycin and azithromycin. Erythromycin is traditionally considered the drug of choice for treating neonatal UU infection; however, the sensitivity of UU strains to erythromycin has declined due to increasing drug resistance and biofilm formation [12]. Azithromycin, has shown effectiveness in clearing UU and reducing the morbidity and mortality associated with BPD [13]. Nonetheless, there is currently no unified standard protocol regarding the optimal dosage, duration of treatment, and safety of medications for neonatal UU treatment, leading to potential treatment uncertainties and risks. In summary, there is no unanimous consensus on the treatment approach for neonatal UU infection, and most clinicians commonly prescribe macrolides empirically [14]. The effectiveness of treatment still relies on the antimicrobial susceptibility profile of the specific region [15]. Therefore, regular monitoring of the regional antibiotic resistance rate of UU, especially in the neonatal population, is essential to guide clinicians in providing effective and safe treatment in clinical settings.

Simultaneous Amplification and Testing (SAT) is a molecular diagnostic method that involves the isothermal amplification of pathogen RNA, enabling the accurate and rapid detection of multiple pathogens [16]. The SAT method can provide test results within 90 min and specifically targets UU RNA to avoid interference from the DNA of dead pathogens. UU RNA testing reflect the status of real-time infection, aids in pathogen elimination assessment during treatment, and helps prevent antibiotic overuse. In this study, we used the SAT method to detect UU in patient samples. The aim was to assess the epidemiological characteristics and clinical antibiotic resistance patterns of UU in this population. A deeper understanding of the epidemiological characteristics and clinical antibiotic resistance patterns of UU can help policymakers develop targeted strategies for preventing and treating UU infections.

Methods

Patients

A total of 8,934 women and children who underwent qualitative detection of UU RNA at West China Second University Hospital (West China Women’s and Children’s Hospital) in Chengdu, China, between March 2019 and September 2023 were included in this study. Urogenital swabs (women) and throat swabs (neonates) samples were collected for SAT testing. The exclusion criteria were as follows: (a) neonates with serious malformations, such as hereditary diseases and congenital heart diseases; (b) patients with other identified pathogens in addition to UU; and (c) patients who were unable to participate in the study for any reason. Broad consent was obtained from all patients before sample analysis. All inspections were carried out in the Department of Laboratory Medicine at West China Second University Hospital (West China Women’s and Children’s Hospital).

Clinical data collection

For women and children, data on age, department of treatment, disease diagnoses, and medication history were collected. For neonates, data on gender, gestational age, birth weight, department for treatment, and disease diagnoses such as preterm birth, low birth weight, intrauterine infection, respiratory diseases (e.g., neonatal pneumonia and BPD), circulatory system diseases (e.g., septicemia and jaundice), digestive system diseases (e.g., NEC and esophageal atresia), nervous system diseases (e.g., intracranial hemorrhage and cephalhematoma) and other relevant conditions were collected. According to the SAT results, the hospitalized neonates were divided into UU positive and UU negative groups, and the incidence of each disease was analyzed. Preterm birth was further classified as preterm birth (≥ 32 weeks, < 37 weeks), very preterm birth (≥ 28 weeks, < 32 weeks), and extremely preterm birth (≥ 24 weeks, < 28 weeks). Low birth weight was further classified as low birth weight (1,500–2,499 g), very low birth weight (1,000–1,499 g), and extremely low birth weight (750–999 g).

Simultaneous amplification and testing (SAT) experiments

For SAT experiments, all samples were promptly placed into a preservation solution to prepare them for testing, following operational guidelines to prevent RNA degradation of pathogenic microorganisms. The samples were stored at a temperature range of 2–8 °C and tested within 24 h using the AutoSAT full-automatic nucleic acid analysis system (Shanghai Rendu Biotechnology Co., Ltd.). A total of 400 µL of the samples were loaded for detection. Sample addition, nucleic acid extraction, amplification, and detection processes were automatically completed within the instrument. Two fluorescent dyes, FAM and VIC, were used for detecting the target gene and internal control, respectively. The qualitative results were assessed by the instrument software and displayed in the result interface. For positive samples, the melting curve was further examined (dt ≤ 35). Samples with dt greater than 35 and less than 40 required retesting. A retest result with a dt less than 40 was considered positive.

Drug susceptibility analysis

This analysis was conducted using the commercial Mycoplasma IST-2 kit (BioMerieux, SA, France) following the manufacturer’s instructions. The kit includes strips for determining antibiotic susceptibility to ofloxacin (OFX), ciprofloxacin (CIP), josamycin (JOS), clarithromycin (CLR), azithromycin (AZM), erythromycin (ERY), pristinamycin (PRI), doxycycline (DOX), and tetracycline (TCY). In brief, the collected specimen was inoculated into 3 mL of R1 solution (transport medium) and mixed with a vial of R2 (lyophilized powder). A 55-µL aliquot of the mixed solution were added to each of the 22 reaction wells on the reagent strip, followed by incubation at 36 °C ± 2 °C for 24 and 48 h. The result was manually interpreted by two experienced senior microbiological technicians based on the color change of the broth. When both low and high concentration reaction wells yield negative results (yellow color), the sample is classified as susceptible. When the low-concentration well yields a positive result (orange-red to red color) and the high-concentration well yields negative results, the sample is classified as inconclusive. When both low and high concentration wells yield positive results, the sample is classified as resistant.

Statistical analysis

The Statistical Package for the Social Sciences, Version 20.0, statistical software was used to analyze frequencies and percentages. Chi-square test was used to compare the incidence of various diseases between UU positive group and UU negative group in neonatal hospitalized patients. Differences were considered statistically significant at a P value less than 0.05.

Results

Women of reproductive age and neonates are the main groups infected with UU

Among the 8,934 patients, a total of 4,281 tested positive for UU (47.92%). Of these positive patients, 28.87% was outpatients, and 71.13% was inpatients (Fig. 1A). Among outpatients with positive UU infections, women aged 20–30 years accounted for 36.25% (448/1,236), and those aged 30–40 years accounted for 51.78% (640/1,236). Different from the outpatients, UU infection was more prevalent among inpatient neonates aged 0–28 days, representing 93.99% (Fig. 1B). Further analysis of the distribution of departments revealed that outpatients were primarily from the departments of gynecology and reproductive medicine, while the majority of inpatients were from the neonatology department (Fig. 1C). The distribution of UU infected patients by department correlated with the age prevalence distribution. These data indicated that UU infections predominantly affected women of reproductive age and neonates. Besides, hospitalization rates due to UU infection were significantly higher in neonates compared to women, highlighting the importance of early detection and treatment in this vulnerable population.

Fig. 1
figure 1

Women of reproductive age and neonates are the main groups infected with Ureaplasma urealyticum(UU). A total of 8,934 specimens were collected to detect UU RNA by Simultaneous Amplification and Testing (SAT). (A) Percentage of UU positive patients and their distribution in outpatient and inpatient departments. (B) Age distribution of UU positive patients in outpatient and inpatient department. (C) Distribution of UU positive outpatients and inpatients in each department. These data indicate that UU infection rates are higher in the southwest China, mainly affecting women of reproductive age and neonates. The hospitalization rate of neonates with UU infection is significantly higher than that of women, highlighting neonatal UU infection as a significant concern

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The incidence of preterm birth and BDP in UU positive neonates is higher than that in UU negative neonates

In a comparative analysis of admission clinical diagnoses between UU positive and UU negative neonates, significant differences were observed in the admission clinical diagnosis of preterm birth, respiratory diseases, intrauterine infections, digestive system diseases, and nervous system diseases. Notably, the incidence of preterm birth in UU positive neonates (1,561/2,959, 52.75%) is higher than that in UU negative neonates (1,900/4,256, 44.64%) (Fig. 2A). Additionally, UU positive patients showed an increasing trend in the incidence of low birth weight, however the difference was not statistically significant (Fig. 2A). In the analysis of gestational age, it was observed that the incidence of very preterm birth and extremely preterm birth was significantly higher in UU positive patients (17.91% and 1.79%, respectively) than in UU negative patients (10.36% and 0.47%, respectively) (Fig. 2B). Regarding the analysis of birth weight, there was an increasing trend in the incidence of low birth weight, very low birth weight and extremely low birth weight neonates in UU positive patients (2.23%, 0.91% and 0.51%, respectively) (Fig. 2C). Furthermore, The incidence rate of BPD was found to be significantly higher in UU positive patients (204/2,959, 6.89%) than in UU negative patients (178/4,256, 4.18%) (Fig. 2D). In addition, in the analysis of the incidence rate of NEC in UU positive and UU negative patients, the difference was not statistically significant (Fig. 2E). Overall, the findings indicate that neonatal UU infection significantly increases the incidence of preterm birth, particularly affecting very preterm and extremely preterm neonates. Notably, the incidence rate of BPD was significantly higher in the UU positive group than in the UU negative group.

Fig. 2
figure 2

The incidence of preterm birth and BDP in UU positive neonates is higher than that in UU negative neonates. A total of 7,215 neonatal inpatients were divided into UU positive group (n = 2959) and UU negative group (n = 4256) according to SAT test results. (A) The incidence of related diseases was compared between the two groups. (B) The proportion of preterm birth was compared between the two groups. (C) The proportion of low birth weight was compared between the two groups. (D) Comparison of BPD incidence rates between groups. (E) Comparison of NEC incidence rates between groups. These findings indicate an increased incidence of very preterm birth and extremely preterm birth in the UU positive neonates, along with a higher occurrence of BPD. Data are presented as mean ± SEM, with P-values determined using the chi-squared test. *p < 0.05; **p < 0.01; and ***p < 0.001

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The sensitivity of UU to azithromycin and erythromycin was different in neonatal, gynecological and obstetric departments

The susceptibility analysis in this study included patients with positive UU cultures who underwent susceptibility testing between 2019 and 2023. Table 1 presents the results of drug sensitivity testing for nine antibiotics, including ofloxacin, ciprofloxacin, josamycin, clarithromycin, azithromycin, erythromycin, pristinamycin, doxycycline, and tetracycline, using UU samples from neonatology, gynecology and obstetrics departments. In the neonatology, the drug susceptibility test results for UU showed higher sensitivity to pristinamycin, doxycycline, tetracycline, josamycin, clarithromycin, azithromycin, and erythromycin (100.00%, 98.66%, 98.21%, 97.32%, 95.54%, 93.75%, and 92.86%, respectively) and lower sensitivity to ciprofloxacin and ofloxacin (8.93% and 13.84%, respectively). In the obstetrics, the drug susceptibility test results for UU showed higher sensitivity to pristinamycin, doxycycline, tetracycline, josamycin, and clarithromycin (100.00%, 98.72%, 98.02%, 97.56%, and 96.17%, respectively) and lower sensitivity to ciprofloxacin and ofloxacin (3.25% and 6.28%, respectively). In the gynecology, UU exhibited higher sensitivity to pristinamycin, doxycycline, tetracycline, and josamycin (100.00%, 99.38%, 96.25%, and 93.17%, respectively) and lower sensitivity to ciprofloxacin and ofloxacin (1.24% and 4.35%, respectively). Overall, UU isolated from various departments consistently showed a pattern of sensitivity to the nine antibiotics, with notable high sensitivity to tetracyclines and macrolides and low sensitivity to fluoroquinolones. However, it is worth noting that the sensitivity of UU to azithromycin and erythromycin in neonatology (93.75% and 92.86%, respectively) was significantly higher than those in obstetrics (75.73% and 80.02%, respectively) and gynecology (59.63% and 69.57%, respectively). These findings suggest that the antibiotic resistance of UU isolated from different departments is not completely consistent.

Table 1 Drug susceptibility analysis of Ureaplasma urealyticum across various departments
Full size table

Discussion

In this study, UU infection was detected in urogenital swabs and throat swabs specimens of patients in southwest China using the SAT method. The objective was to gain a better understanding of the current epidemiological characteristics and clinical antibiotic resistance patterns of UU infection among women and children in southwest China. In this study, we found that the total positive rate of UU was 47.92%, with a higher prevalence among women of reproductive age and neonates. Regarding the prevalence of UU across different age groups, UU infection was more prevalent in women of reproductive age (20–40 years) among outpatients, while it was more prominent in neonates (0–28 days) among inpatients. In terms of departmental prevalence, UU infection was more common among outpatients in the gynecology and reproductive medicine, while it was prominent among inpatients in the neonatology. These findings are consistent with previous studies, suggesting that women of reproductive age and neonates are the main populations affected by UU infection [17,18,19]. Besides, neonates were the main population of UU positive inpatients, highlighting the importance of early detection and treatment in this vulnerable population. In the analysis of admission clinical diagnoses of neonatal inpatients, an increased incidence of preterm birth and low birth weight was observed in the UU positive group, particularly among very preterm and extremely preterm neonates. Previous studies have consistently reported that UU can contribute to adverse pregnancy outcomes, such as preterm birth and low birth weight [20,21,22,23,24]. Our findings further support the association between UU and adverse pregnancy outcomes. However, the pathogenic role of UU in pregnancy remains controversial, as UU can also be part of the normal vaginal flora [25]. Currently, the mechanism by which UU infection impacts pregnancy is not fully understood, and UU presence in the placenta does not consistently correlate with inflammation and adverse outcomes. Possible explanations for these observations may include variations in the timing and duration of colonization, differences in virulence among serovars/strains, and modulation of maternal immune responses leading to either suppression or exacerbation of the infection [19, 26]. Further research is needed to investigate the mechanism by which UU infection impacts pregnancy outcomes. In Fig. 2, it is evident that among hospitalized neonatal patients, the incidence rate of BPD was significantly higher in the UU positive group than in the UU negative group. Regarding BPD, a prospective multicenter study identified UU colonization as a significant risk factor for BPD development, even after surfactant administration [27]. Similarly, a meta-analysis demonstrated a significant association between UU colonization and the development of BPD in preterm neonates [28]. Neonates, being a vulnerable population, exhibit diverse clinical manifestations following UU infection due to the immature development of multiple organ systems. They are at a higher risk of experiencing serious complications, including preterm birth, low birth weight, BPD, NEC, and long-term issues like asthma and cerebral palsy. Therefore, in order to effectively prevent adverse pregnancy outcomes and neonatal complications, it is essential to conduct UU screening tests for women before pregnancy and for neonates.

In the study of antibiotic sensitivity, we observed that UU demonstrated sensitivity to pristinamycin, doxycycline, tetracycline, and josamycin. Regardless of the age group or department, more than 90% of the tested samples exhibited sensitivity to these antibiotics. The findings align with those previously reported [17, 29, 30]. On the contrary, our investigation into the sensitivity of UU isolates in gynecology and obstetrics departments to ofloxacin and ciprofloxacin revealed sensitivities lower than 10%. This sensitivity was notably lower than the reported sensitivities of UU isolates to ofloxacin (34.1% and 19.1%, respectively) and ciprofloxacin (5.3% and 14.5%, respectively) in studies conducted by Song et al. and Lee et al [17, 29]. The variation in antibiotic sensitivity profiles of UU isolates can be attributed to the lack of a standardized antimicrobial treatment protocol for UU infection, leading to varying antimicrobial agent selections across different regions [14, 31]. The effectiveness of current treatments heavily relies on the antimicrobial sensitivity patterns specific to each region [15]. Further research and refinement are required to establish a unified standard for antimicrobial therapy in UU infections. Although UU isolates obtained from gynecological, obstetrics, and neonatology departments have shown high sensitivity to tetracyclines, these antibiotics are not widely used in neonatal and obstetrics settings compared to gynecological settings due to potential side effects. Macrolides remain the preferred treatment options for pregnant women and neonates. Additionally, it is worth noting that neonatal UU infection predominantly occurs through vertical transmission from the mother. However, our drug susceptibility analysis revealed significant differences in the sensitivity of UU isolates from neonatology, obstetrics, and gynecology departments to azithromycin and erythromycin. This underscores the necessity for continuous monitoring of UU sensitivity to various antibiotics in diverse populations to guide effective clinical treatment strategies. Based on drug sensitivity data, different antimicrobial agents should be used to treat UU infection empirically in various patient groups. Our drug susceptibility results indicate that the recommended first-line options are doxycycline, tetracycline, pristinamycin, and josamycin for women, josamycin and clarithromycin for pregnant women, and erythromycin and azithromycin for neonates [17, 29].

The study has some limitations that should be acknowledged. First, the small sample size of neonatal UU infected patients in this retrospective study limited the analysis of differences in adverse outcomes after infection. Although there was an increasing trend in these outcomes, the differences did not reach statistical significance. Therefore, further studies on a larger sample size for analysis are required to further verify this upward trend. Second, although we observed varying levels of resistance among UU isolates to azithromycin and erythromycin across departments, we did not provide an explanation for this variation. Further research is required to investigate this variation.

Conclusion

In conclusion, in view of the high incidence of UU infection in southwest China, we recommend maternal screening for UU as done for Group B Streptococcus (GBS) infections, in order to offer preventive treatment. It is also important to continuously monitor the sensitivity of UU to antibiotics in different populations and regions to ensure effective antibiotic treatment. The implementation of this study may contribute to a better understanding of the epidemiological characteristics and antibiotic resistance patterns of UU infection among women and children in southwest China, which can aid in the development of more effective interventions, prevention strategies, and treatments for UU infection.

Data availability

All data generated or analyzed during this study are included in this published article.

Abbreviations

UU:

Ureaplasma urealyticum

SAT:

Simultaneous amplification and testing

BPD:

Bronchopulmonary dysplasia

NEC:

Necrotizing enterocolitis

OFX:

Ofloxacin

CIP:

Ciprofloxacin

JOS:

Josamycin

CLR:

Clarithromycin

AZM:

Azithromycin

ERY:

Erythromycin

PRI:

Pristinamycin

DOX:

Doxycycline

TCY:

Tetracycline

GBS:

Group B Streptococcus

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Acknowledgements

Not applicable.

Funding

This work was supported by Sichuan Science and Technology Program (Grant No. 2023YFS0186 and 2023YFS0222) and the Clinical Research Foundation of West China Second University Hospital (Grant No. KL066 and KL076).

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Author notes

  1. Meng-ke Huang, Yun-long Yang and Lu Hui contributed equally to this work.

Authors and Affiliations

  1. Department of Laboratory Medicine, West China Second University Hospital, Sichuan University, No. 20, Section 3, Renmin Road South, Chengdu, Sichuan, 610041, P. R. China

    Meng-ke Huang, Yun-long Yang, Lu Hui, Xiao-lin Chen, Ting Liu & Yong-mei Jiang

  2. Key Laboratory of Birth Defects and Related Diseases of Women and Children (Ministry of Education), West China Second University Hospital, Sichuan University, Chengdu, China

    Meng-ke Huang, Lu Hui, Ting Liu & Yong-mei Jiang

  3. State Key Laboratory of Biotherapy and Cancer Center, National Collaborative Innovation Center for Biotherapy, Sichuan University, Chengdu, China

    Ting Liu

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Contributions

MKH drafted the manuscript. XLC, YLY, and LH participated to the acquisition of data. MKH and TL generated the experimental results. TL and YMJ designed the study and reviewed the manuscript for intellectual content. All authors read and approved the fnal manuscript.

Corresponding authors

Correspondence to Ting Liu or Yong-mei Jiang.

Ethics declarations

Ethics approval and consent to participate

This study was approved by the Medicine Ethics Committee of West China Second University Hospital, Sichuan University (NO.2019-18). Broad consents were acquired before SAT analysis. For drug susceptibility analysis, we obtained the data from the Medical Records and Statistics Room hence informed consent waiver for this part of the study is approved by Medicine Ethics Committee of West China Second University Hospital, Sichuan University. We confirm that all methods were performed in accordance with the relevant guidelines and regulations.

Consent for publication

All authors approved the final version of the manuscript. All the authors have accepted responsibility for the entire content of this submitted manuscript and approved submission.

Competing interests

The authors declare no competing interests.

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Huang, Mk., Yang, Yl., Hui, L. et al. Epidemiological characteristics and clinical antibiotic resistance analysis of Ureaplasma urealyticum infection among women and children in southwest China. BMC Infect Dis 24, 849 (2024). https://doi.org/10.1186/s12879-024-09760-9

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  • DOI: https://doi.org/10.1186/s12879-024-09760-9

Keywords

BMC Infectious Diseases

ISSN: 1471-2334

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