Jialin Li
Lesen Liu3†
Xiang Ma- 1Department of Respiratory Disease, Children's Hospital Affiliated to Shandong University, Jinan, Shandong, China
- 2Jinan Key Laboratory of Pediatric Respiratory Diseases, Jinan Children’s Hospital, Jinan, China
- 3Surgical Department, Huaiyin People’s Hospital, Jinan, China
With the widespread use of macrolide antibiotics in China, common pathogens causing children’s infections, such as Streptococcus pneumoniae, Streptococcus (including Group A streptococcus, Group B streptococcus), Staphylococcus aureus, Bordetella pertussis, and Mycoplasma pneumoniae, have shown varying degrees of drug resistance. In order to provide such problem and related evidence for rational use of antibiotics in clinic, we reviewed the drug resistance of common bacteria to macrolides in children recent 20 years.
Introduction
Macrolides (MLs) are a diverse class of hydrophobic compounds characterized by a macrocyclic lactone ring that typically contains at least 12 elements and distinguished by variable side chains/groups. The 23S rRNA in 50S subunit in bacterial ribosome contains a peptidyl transferase (PTC) that catalyzes peptide bond formation to link amino acids into proteins. MLs interact with the nucleic acid in the domain V of the catalytic center of the enzyme, bind to the part between PTC and nascent peptide exit tunnel and then block the channel to inhibit the synthesis of bacterial proteins, which finally playing an antibacterial effect (Vázquez-Laslop and Mankin, 2018). In addition to antibiotic properties, MLs also have been shown to display antiviral, antiparasitic, antifungal, and immunosuppressive actions. So, they were widely used in clinical.
However, with the widespread use of these drugs, many bacteria are showing a tendency to become more resistant to the drugs. The mechanisms of ML resistance mainly include the following: 1.erm-mediated rRNA methylation: it is mainly caused by the double methylation of 23S rRNA in bacteria. Methylation can reduce the affinity of MLs to the ribosome site to one hundred thousand times of the previous, and is completed by erm enzymes (Farrell et al., 2003). 2. rRNA mutation: such as A2058U/A2058G in 23S rRNA in Streptococcus pneumoniae or A2064G/A2064G in 23S rRNA in Mycoplasma pneumonia (Farrell et al., 2004; Lu et al., 2020). 3. Efflux mediated by mef: mef encodes an efflux pump, which can use MLs as a substrate to expel drugs from the bacteria by consuming energy, thereby reducing the sensitivity of bacteria to drugs (Farrell et al., 2003). 4. Ribosomal protein variants: the most important ones are L4 and L22 (Farrell et al., 2004).
In China, the resistance of many bacteria to MLs is on the rise. Here, we review the situation of drug resistance in China in the past 20-30 years. Search strategy: We searched PubMed, Wanfang database, Zhiwang of China, Google Scholar for articles published before 31 December 2022, by use of the terms: “Streptococcus pneumoniae”, “Mycoplasma pneumoniae”, “Bordetella pertussis”, “Staphylococcus aureus”, “ Group A Streptococcus/Streptococcus pyogenes”, “ Group B Streptococcus/Streptococcus agalactiae,” AND “macrolide” AND “resistance”, and reference lists of identified studies. Only articles written in Chinese and English were included. Finally, only the most relevant papers for this review were cited. The characteristics of the included literatures are shown in the Supplementary Table 1.
Streptococcus pneumoniae
SP is the most important pathogen in otitis, sinusitis, bronchitis, and community-acquired pneumonia (CAP), as well as a predominant cause of meningitis and bacteremia. The widespread use of MLs is associated with increased resistance. Reports of SP resistance to MLs first appeared in the 1980s–1990s globally and the first report of macrolides-resistant SP (MRSP) in China was also in 1980s (Ye et al., 1988).A total of 295 invasive SP strains were identified from 18 provinces of China during 1981-1983 in that study. Only one of them was resistant to erythromycin (ERY), with a resistance rate of 0.34% (1/295). Since then, domestic studies have found a significant increase in prevalence of MRSP. Li (Li et al., 1999) found that resistance to ERY of SP increased from 2% in the mid-1980s to 79% in the mid-1990s, and clarithromycin (CLA) from 2% in the mid-1980s to 76% in the mid-1990s. In 1997 (Yu et al., 2000), 76.8% of SP were found to be resistant to ERY and children who had taken the drug in the last month were more likely to carry ERY-resistant strains (39 vs 27%, RR 1.5, 95% CI 1.1-2.0). Then, the continuous monitoring in 1998-2000 showed that the ERY resistance rates of the SP in Beijing were 82.2% and 87.4%, respectively (Yu et al., 2001). In addition to Beijing, the increasing resistance rate were also reported in Shanghai (Zhang et al., 2000). The data from Europe for 1992-1998 showed that more than 40% of isolates from France and Italy were resistant to MLs, whereas less than 10% of isolates from Germany, the Netherlands, the Czech Republic, and Poland (Schito et al., 2000), which was lower than China in the same period.
At the turn of the century, Yang (Yang et al., 2002b) carried out drug sensitivity test of SP isolated from nasopharyngeal specimens of children with upper respiratory tract infection in Beijing, Shanghai, Guangzhou and Xi’an. They reported that the resistant rate of 624 isolates to ERY ranged from 75.4% to 96.7%, and 80-99% of the resistant isolates had minimum inhibitory concentration (MIC) ≥256μg/ml. At the same period, they also (Li et al., 2013) reported that 119 of 120 (99.2%) SP with serotype 19F showed resistant to ERY. Of the 119 ERY non-susceptible pneumococci, ermB and mefA were detected in 115 (96.6%) and 64 (53.8%) isolates, respectively. Both ermB and mefA were detected in 60 (50.4%) strains. Even more frustrating, 96.6% strains had MIC >256μg/ml. Subsequently, a large number of single and multi-center studies showed that the resistance rate of SP to MLs was in the range of 79%-100% (Liu et al., 2008; Wang et al., 2008; Zheng et al., 2009; Chen et al., 2010b; Xue et al., 2010; Xiong et al., 2012; Zhang et al., 2013c). Only a few single-center studies (Li et al., 2012; Jiang et al., 2013) have shown low rates of resistance to ERY (20%-21.7%). And the resistance rate was lower in adults (69.2%-73.3%) than in children over the same period (Li et al., 2003; Yao et al., 2005; Yang et al., 2008). The Prospective Resistant Organism Tracking and Epidemiology for the Ketolide Telithromycin (PROTEKT) data (1993-2003) also showed a global increase in Mls resistance of SP, from 31% in 1999 to 36.3% in 2003 (Schito and Felmingham, 2005). But, Felmingham collected 20,142 SP isolated from 151 centers in 40 countries between 2001 and 2004, and found there that was no significant temporal trend in the prevalence of MLs resistance in any country. The highest rates (~80%) were recorded among isolates collected in the Far East, followed by South Africa (~54%) and Southern Europe (~37%), whereas resistance was lowest in Latin America (~15%), Australia (~18%) and Northern Europe (~18%). And, telithromycin exhibited good antibacterial activity against SP. The most common macrolide resistance genotype among SP was erm(B) (~58%), followed by mef(A) (~30%). (Felmingham et al., 2007).
Since 2010, the resistance of MLs has increased even more, with many studies reporting a resistance rate of>92% (Zhao et al., 2017; Fu et al., 2018; Du et al., 2021; Liang et al., 2021; Liu et al., 2021b). One recent study (Zhou et al., 2021) even showed that more than 90% of the strains were resistant to azithromycin (AZM), CLA, and ERY. It is worth noting that MIC50 and MIC90 of AZM, CLA, and ERY were all>1024μg/ml. Only Shenzhen reported a slight downward trend in SP resistance to MLs (Li et al., 2019c). During this period of time, there was no significant difference in drug resistance between invasive SP and non-invasive SP strains, that is to say, both invasive and non-invasive strains showed high resistance to MLs (Huang et al., 2015b; Lyu et al., 2016; Wang et al., 2019a). Meanwhile, data from China Antimicrobial Surveillance Network (CHINET) (CHINET, 2023) since 2006 showed that both penicillin-sensitive and non-sensitive non-meningitis SP show high resistance rate to MLs (80.2%-100%). Furthermore, 143 of the 144 (99.3%) serotype 14 SP isolates resistant to ERY and the ermB gene was determined in all ERY resistant isolates (100%), and the mefA gene was positive additionally in 13 of them (9.03%) (He et al., 2015). Meanwhile, studies around the world have showed that macrolide resistance among SP is geographically variable but ranges from <10% to >90% of isolates (Pan et al., 2015; Xiao et al., 2015).
In a word, the onset time of macrolide resistance in SP is basically the same as that in other countries in China. In the past 30 years, the resistance of SP to MLs in children in China has shown an increasing trend, especially in the 1990s, when a sharp upward trend occurred, and then maintained at a high level. ermB and mefA genes are major SP of resistant to MLs.
Staphylococcus aureus
SA is an aerobic or facultative anaerobic gram-positive coccus. With strong pathogenicity, it can cause a variety of infections including severe sepsis, pneumonia and wound infection. A growing number of studies have reported that the bacterium is resistant to a variety of antibiotics, especially MLs (Chen et al., 2022).
Resistance to MLs in SA was rarely reported in China before 2000. Huang (Huang and Liu, 1990) compared the resistance rate of SA between 1979-1984 and 1985-1988 in Chongqing, and earlier concluded that the drug resistance rate of ERY increased (P<0.05). Studies in several other southern provinces have also found significant increases in MLs resistance (from 72% to 100% in Guangdong, from 11.1% to 65.8% in Anhui) (P<0.05) (Zhang et al., 1998; Jin et al., 1999; Li and Xiong, 2001). In Beijing, Fan and Ma reported high rates of (79.7-90.3%) MLs resistance (Fan et al., 2000; Ma et al., 2000) and they also found that the resistance rate of methicillin-sensitive SA (MSSA) to ERY was significantly lower than that of MRSA (81% vs 97.1%) (Fan et al., 2000). Meanwhile, data from Guangdong showed that all the 58 MRSA isolated from 1990 to 1995 were resistant to ERY (Zhou, 1997). Prior to 2000, only SA from newborns in Shanxi province in 1995-1997 was reported to have a resistance rate of less than 50% to ERY (Guo et al., 2000). Many reports based on blood samples found that the resistance to ERY fluctuated between 63% and 76% (Duan et al., 2000; Huang and Chen, 2001; Xu and Shao, 2002). It has been reported that the detection rate of SA in sepsis children decreased from 35.4% in 1991 to 5.3% in 2000 (P<0.005) (Xu and Shao, 2002), but no decrease in the resistance of SA to MLs was found. In a word, it is clear that SA showed a significant upward trend in resistance to MLs before 2000. However, H.Westh studied 718 cases of bacteremia with MRSA, occurring between 1959 and 1988 and found that MRSA resistance to MLs occurred at a stable low level (13%) during the whole observation period and always had high MICs to ERY (Westh et al., 1991).
Since 2000, the number of studies on SA resistance to MLs gradually increased. Wang (Wang et al., 2008) monitored the resistance of 7835 SA isolated from children during 2000 to 2006, and found that the resistance rate of ERY was 66.39% and showed an increasing trend (P<0.001). Two studies bases on respiratory specimens in children showed that the resistance rates of SA to ERY was between 45.6%-58.1% (Wu J. et al., 2013) and 77-86.7% (Xia et al., 2012). Two other studies (Zhao et al., 2012a; Chen et al., 2017) found a decrease in the rate of resistance to ERY in SA (81.9-68.2% and 81.9%-54.7%), but the level of MIC was high (MIC90s ≥ 256ug/ml) (Zhao et al., 2012a). At the same time, some studies reported low resistance rate in some areas. For example, the resistance rate of SA to ERY from children in Hangzhou during 2001-2002 was 37.93% (Hua et al., 2003) and it was only 24.5% in Qinghai during 2009 to 2010 (Long and Wang, 2012). Moreover, the date from Zhejiang province from 2007 to 2010 showed low resistance rates of 11.1%, 20.0% and 25.9% (Sun, 2011). In this decade, there have been more studies to compare the resistance of MRSA and MSSA. Almost all studies have shown that the resistance of MRSA to ERY was significantly higher than that of MSSA, regardless of the type of specimen (Hu and Xia, 2009; Shi and Jian, 2010; Wang et al., 2011b; Wang, 2013; Zhang et al., 2013a). Similar findings were made for AZM resistance (Zhang and Jin, 2013). A deeper study (Wang et al., 2011a) found that the resistance rate of MRSA to ERY was as high as 97.9%, and MIC50 and MIC90 were both higher than 256ug/ml. They also found that MRSAs carrying type IV or V SCCmec often showed multiple resistance. In conclusion, from 2000 to 2010, the resistance rate of SA to MLs showed a trend of fluctuating increase and then decreasing. MRSA had a higher resistance rate to MLs than MSSA. In Belgium, Olivier Denis found the resistance of 455 clinical MRSA strains to ERY was 64% (Denis et al., 2004).
Since 2010, the research on the resistance of SA to MLs has been more extensive and in-depth. Continuous monitoring from several regions in China showed that the resistance of SA to MLs was on the rise (Huang et al., 2014; Li et al., 2016; Wu et al., 2019; Bao et al., 2021; Ding and Li, 2022). However, the data from CHINET (CHINET, 2023) showed that the resistance rates of MLs in MSSA and MRSA both showed a fluctuating downward trend. And some studies have shown a wide range of resistance rates, making it not easy to draw the conclusion that the drug resistance rate increases or decreases (Zhai et al., 2016; Chi et al., 2018). During this period, there were many studies on the resistance of MRSA and MSSA to MLs, and most studies showed that the resistance rate of MRSA (73.2%-100%) was significantly higher than that of MSSA (16.3%-66.1%) (Huang et al., 2015a; Li et al., 2016; He et al., 2017; Chi et al., 2018; Min et al., 2019; Zhao et al., 2020; Xiao et al., 2021; Zhou et al., 2022). Hu (Hu et al., 2016) reported that the resistance rate of CA-MRSA to ERY in Shenzhen in 2014 was 81.4% and that of HA-MRSA was 86.7%s. Chen (Chen et al., 2022) reported 60% resistance to ERY in CA-MSSA, 86% in CA-MRSA, 55% in HA-MSSA, and 82% HA-MRSA in 2015-2017. In addition to this, the data from the Chinese Pediatric Infectious Disease Surveillance Program (ISPED) (Fu et al., 2021) showed that the resistance rate of MRSA (n=11128) and MSSA (n=20667) to ERY from 11 children’s hospitals during 2016-2020 was 78.2% and 51.9%, respectively. And the data of CHINET (CHINET, 2023) also showed that the resistance rates of MLs in MSSA ranged from 43.9% to 55.3%, while those in MRSA ranged from 93.4% to 73.2%. Antibiotic Resistance Monitoring in Ocular Microorganisms(ARMOR) reported 59.7% of SA isolates overall were resistant to MLs between 2009-2018 (Bispo et al., 2022), which was lower than China.
There have also been studies of resistance in SA from different sources of samples, but no significant differences have been found. Specimens from skin, soft tissue, pneumonia, pus, etc., all showed high (62.3%-98.5%) drug resistance rates (Deng et al., 2012; Deng et al., 2013; Ning et al., 2014; Zhang et al., 2014a; Ran et al., 2017). Some studies also analyzed resistance rates in both children and adults, but the results are not very clear. For example, a recent study (Li et al., 2020b) found lower rates of ERY resistance in adult than in childhood (36.60% vs 46.31%, P<0.05). However, Ma (Ma et al., 2007) reported that the resistance rate of SA from adults to ERY was 89.8%, while that from children was 49.0%. Two other studies analyzed the causes of MLs resistance. Li (Li et al., 2020b) found that the resistance rate of Class I integron-positive isolates to ERY was higher than that of class I integron-negative isolates (50.85% vs39.29%, P<0.05). Chen (Chen et al., 2014a) reported that the mecA positive strain had a higher resistance rate to ERY than that of negative strain (80.30% vs 35.0%).
From the literature above, we can see that the research on the resistance of SA to MLs first experienced a rapid rising and then showed a decreasing trend of volatility, with certain regional differences in China. And, the resistance rate of MRSA was higher than MSSA.
Group A streptococcus
GAS, alternatively termed Streptococcus pyogenes, is a Gram-positive pathogen that routinely causes a variety of non-invasive (pharyngitis, impetigo, cellulitis, etc) and invasive infections (necrotising fasciitis, sepsis, etc). MLs is an important treatment for GAS infections. In the present study, we investigated trends in GAS resistance to MLs in China.
In 1968, a strain of GAS resistant to ERY isolated from a throat swab in a child was reported for the first time in the world (Sanders et al., 1968). In Europe, the ML resistant-GAS strain first appeared in Spain in the 1990s, and despite this, studies in Spain since then have shown that GAS has a resistance rate of 0% to ERY (Ardanuy et al., 2010). The first drug susceptibility test in mainland China was conducted by Su (Su et al., 2003), who collected 620 strains from Guangzhou, Jilin, Hubei and Chongqing during 1988-1994. The resistance rate of GAS to ERY was 35.2%. Later, Dong (Dong et al., 1999) collected strains from various provinces and cities during 1993-1994 and found that the resistance rate of ERY was different in different regions: 75.26% in Jilin, 22.22% in Sichuan, 1.1% in Hubei, and 27.19% in Guangzhou. In addition to differences in drug resistance between different cities, Dong (Dong et al., 2001) found that there were also differences between urban and rural areas: during 7 consecutive years of surveillance, GAS resistance to ERY in rural children in Guangzhou (21.4%-67.4%) was much more severe than that in urban children (4.4%-23.8%). Lin (Lin et al., 2010) reported that the resistance rate of GAS to telithromycin also showed an increasing trend, from 20.37% during 1993-1994 to 87.93% during 2005-2008. Similarly, the resistance rate of Josamycin (JOS) increased from 84.8% in 1993-1994 to 98.1% in 2005-2008 and the CLA resistance rate of GAS in Beijing area during 1993-1994 was 79% (Wu et al., 2014). In a word, the GAS resistance rate of MLs in China before 2000 was relatively high, although there were regional differences.
Deng (Deng et al., 2008) collected 47 strains in children with impetigo from 2005 to 2007 in Beijing, and the resistance rate of ERY was 47.1%. In 2009, a total of 265 GAS strains were collected from 14 hospitals, of which 82.1% were resistant to ERY (Wang et al., 2010). During the same period, many multi-center studies showed that the resistance rate of ERY in Beijing, Shanghai, Liaoning, Sichuan, Shenzhen were all above 90% (Liang et al., 2008; Liu et al., 2009; Chang et al., 2010; Chen et al., 2012; Ji et al., 2012; Zhou et al., 2014a). Meanwhile, the drug resistance rate of AZM in Beijing, Tianjin and other areas were also higher than 95% (Liang et al., 2008; Liu et al., 2009; Chang et al., 2010; Ji et al., 2012; Yin et al., 2018). Other kind of MLs were also at high drug resistance levels. For example, the resistance rates of GAS from Beijing, Shanghai, Chongqing, Tianjin to CLA were all >90% (Liang et al., 2008; Ma et al., 2008; Liu et al., 2009; Chang et al., 2010; Feng et al., 2010a; Ji et al., 2012; Wu et al., 2014; Yin et al., 2018) and the resistance rates of roxithromycin and doxomycin are also ≥90% (Han et al., 2007; Ma et al., 2008; Feng et al., 2010a). In conclusion, the data from 2000-2010 in China show that the resistance rate of GAS to MLs is on the rise, especially after 2005. However, a decline in the rate of resistance to ERY in GAS in several abroad regions was reported after 2005 (<10%) (Ardanuy et al., 2010; Montes et al., 2014; Berbel et al., 2021).
After 2010, the resistance rate of GAS to MLs remained high. Wang (Wang et al., 2013a) reported that 71 strains collected in Beijing in 2011 were all resistant to ERY (100%). Also in Beijing, Zhu (Zhu et al., 2021) collected a total of 234 strains from 2013 to 2019, and the resistance rate of ERY was as high as 98.29%. Sun (Sun et al., 2022) compared the ERY resistance rate of 50 strains in Shenzhen from 2016 to 2020, and it was all>96% in the other years except for 92% in 2017. In 2017, the resistance rate of 66 strains to ERY in a hospital in Guangzhou was as high as 96.97% (Tan et al., 2019). It has been reported that 35 GAS strains cultured from throat swabs of children in Beijing were 100% resistant to mediamycin, and the resistance rate to acetylspiramycin was 97.14% (Yang et al., 2015a). In Asia, in addition to China, Japan also has a high rate of MLs resistance (Tatara et al., 2020; Ikebe et al., 2021).
There are few studies on GAS resistance genes in China. The earliest strains related to GAS resistance genes in mainland China came from 2003 (Chang et al., 2010). Of 91 MLs resistant isolates, 77 (84.6%) had the ermB gene, while 14 isolates (15.4%) had the ermA gene. Ji (Ji et al., 2012) collected 52 strains from children with impetigo from 2003 to 2008 in Beijing, among which 92.3% carried ermB and 7.7% carried ermA. In addition, ermB genes accounted for more than 90% of the strains from Beijing, Shanghai, Shenzhen, and Guangzhou before 2010 (Deng et al., 2008; Ma et al., 2008; Feng et al., 2010a; Feng et al., 2010b). A study from Shandong after 2010 showed that the ermB gene accounted for up to 100% of all strains (Liu et al., 2015).
To sum up, the resistance of GAS to MLs in China shows an obvious upward trend, with some fluctuations, and the resistance varies in different regions. ErmB gene is an important gene for GAS resistance to MLs, and it is dominant in China.
Group B Streptococcus
GBS, also known as Streptococcus agalactiae, is a β-hemolytic Gram-positive bacterium that colonizes the lower genital tract as an asymptomatic microbe. However, it can be highly pathogenic if it was established in other host niches. During pregnancy, ascending GBS infection is associated with preterm birth, stillbirth, and fetal injury. In addition, fetuses and neonates are uniquely susceptible to GBS infections, which most commonly include sepsis, pneumonia, meningitis, and encephalopathy. MLs are one of the first-line treatments for GBS. In the past decades, resistance to MLs continue to rise all over the world.
The earliest article on the resistance of GBS to ERY in China was published in 1989 (Cao et al., 1989). They obtained vaginal secretions of pregnant women and skin wipes of newborns from Beijing. A total of 10 strains of GBS were cultured and no ERY resistant strains was found. Only 2 years later, Zhang (Zhang et al., 1995) reported 53 strains also from pregnant women and newborns, and the resistance rate to ERY was as high as 66.04%. However, a susceptibility test of the GBS strain in Australian in 1999 showed that the ERY resistance rate was only 2.8% (Stylianopoulos et al., 2002). Shen (Shen et al., 2005) reported that the resistance rate of GBS to ERY was 8% in Beijing in 1998, increased to 16% in 1999, and 45% in Guangzhou in 1999, which was significantly higher than that in Beijing (p<0.01). Of the 45 ERY-resistant isolates, 44% contained ermB and 29% contained mefA, 13.33% contained both ermB and mefA genes. Yang (Yang et al., 2002a) compared the resistance of 113 GBS from Beijing (n=69) and Guangzhou (n=31), China, and St. Petersburg (n=13), Russia between 1996 and 1999. Forty-six percent of the isolates from China were ERY resistant while the isolates from Russia were all susceptible. The ermA gene was detected only in Beijing strain. Thirty-four strains (30.1%) carried ermA and/or ermB, of which 33 (97.1%) strains were resistant to ERY, no ermC gene was found. However, 53 strains carrying mreA, 18 strains carrying mefA, and 1 ermA positive strain were still sensitive to ERY. Two resistant strains did not carry any detected genes (mreA, mefA and ermA/B/C). In Canada, a study of 32 ERY-resistant GBS strains were genotyped and 88% were found to be erm positive (54% constitutive) and 12% mef positive (De Azavedo et al., 2001).
It was reported that only 8.6% of 46 strains of GBS isolated from maternal cervical secretions and neonatal pharyngeal during 2003-2006 were resistant to ERY (Zhao et al., 2007). Among 193 strains isolated from throat swabs of children and vaginal secretions of pregnant women in Jingdezhen between 2004 and 2008, the ERY resistance was also only 15% (Lin et al., 2015). However, Guo (Guo et al., 2012) reported that the resistance rate of ERY in Zhejiang Province was as high as 86.2% in 2006, 86.1% in 2007, and 84.8% in 2010. A number of studies (Guo et al., 2012; Li et al., 2015; Lin et al., 2015; Zhang et al., 2015b; Lin et al., 2022a) comparing the changes in GBS resistance rates in different years suggested that the high ERY resistance rate in the 10 years from 2001 to 2010, most of which fluctuated between 41% and 93.3%. The study (Chen et al., 2010a) from Guangzhou also showed that ermB gene expression accounted for 71.1%, mefA 52.2% and mefE 68.9% in ERY resistant strains.
There has been an increase in research on GBS resistance since 2010. Studies in children mainly focused on invasive infections in neonates, and most of these studies have been based solely on blood specimen (Wu X. et al., 2013; Chen et al., 2014b; Huang et al., 2018; Wang et al., 2018; Yu and Hu, 2018; Zhan et al., 2018; Liang and Wang, 2019; Liu et al., 2019; Xie and Liu, 2020; Liu et al., 2021a; Lin et al., 2022a; Qu et al., 2022), with a few studies on other specimens, such as cerebrospinal fluid (CSF) and sterile body fluid (Huang et al., 2016; Li et al., 2019a). These studies have shown that the rate of ERY resistance among invasive GBS strains has fluctuated between 43.33% and 100% (Wu X. et al., 2013; Chen et al., 2014b; Huang et al., 2018; Wang et al., 2018; Yu and Hu, 2018; Zhan et al., 2018; Liang and Wang, 2019; Liu et al., 2019; Xie and Liu, 2020; Liu et al., 2021a; Lin et al., 2022a; Qu et al., 2022), among which only two studies (Huang et al., 2018; Liang and Wang, 2019) from Shanghai and Zhejiang province showed that GBS resistance to ERY was less than 50%. A multi-center continuous monitoring in southern China (Li et al., 2019a; Li et al., 2020a) showed a fluctuating upward trend in the resistance rate of ERY (66.7 in 2013 to 78.6% in 2016). They also found that 48 of 56 (85.7%) ERY resistant strains carried the ermB gene and two (3.6%) strains carried both ermB and mefA. However, it should be noted that 100% of the 17 intermediate strains carried ermB and 5.9% also carried mefA. In the United States, ERY resistance rates are also high in the GBS strains that cause invasive adult and neonatal disease, at 54.8% and 44.8%, respectively (Francois Watkins et al., 2019; Nanduri et al., 2019).
In addition to neonates, studies (Lei et al., 2015; Wang et al., 2015a; Zhang et al., 2015a; Zhong et al., 2015; Li et al., 2018c; Lin et al., 2019; Wang et al., 2019b; Li et al., 2020a) on the resistance of GBS strains isolated from infants and young children were also mainly derived from invasive infection strains. Among these studies, only one study (Zhang et al., 2015a) from Shenzhen reported that the resistance rate of ERY was 41% and the intermediate rate was 25%. Other studies all showed that the resistance rate of ERY was higher than 75%, the highest was 92.5% (Wang et al., 2015b) and MIC50-90 was higher than 256μg/ml. Similarly, most AZM resistance rates have been above 95% since 2010 (Wang et al., 2015a; Wang et al., 2015b; Wang et al., 2020). The earliest study on the resistance rate of CLA can be traced back to 2008. Wang (Wang et al., 2015a) collected 40 strains in Shenzhen and Beijing from 2008 to 2013 and found that 92.5% of the strains resistant to CLA. So far, studies on the CLA resistance rate of GBS from different regions in China are all lower than this value, but the overall resistance rate is still high. For example, Zhang (Zhang et al., 2018) reported that the resistance rate of GBS to CLA in Kunming, Yunnan Province was 42.5%, which is the lowest reported level in China. The study on the resistance rate of GBS to telithromycin was relatively late and rare. It was reported that the resistance rate of 40 strains during 2008-2013 was 0 (Zhong et al., 2015), and 48 strains isolated during 2013-2014 was 30.56% (Wang et al., 2015a). Studies on the detection of resistance genes increased during this decade, with the ermB gene accounting for more than 80% in Guangzhou, Beijing, Shanghai and Jiangxi province (Li et al., 2018a; Li et al., 2018b; Nie et al., 2018; Li et al., 2019a; Du, 2022). In Sub-Saharan Africa, a meta analysis shows the resistance rate of ERY was only 25.11% (Wadilo et al., 2023).
In conclusion, the resistance rate of GBS to MLs has remained at a high level in China, with the ermB gene dominant.
Bordetella pertussis
BP is the responsible pathogen of pertussis, an acute respiratory infectious disease that occurs in children usually and causes paroxysmal, spasmodic cough. MLs represented by ERY have been the first choice for the prevention and treatment of pertussis. The first ML-resistant BP (MRBP) strain was reported in 1994 in a 2-month-old infant in Yuma, Arizona, US (Lewis et al., 1995). Since then, countries such as the United Kingdom, France, Iran and even East Asian and Southeast Asian countries including Japan, Vietnam and Cambodia, have reported the appearance of MRBP, but the prevalence in these countries is generally low (0.5% to 18.2%) (Korgenski and Daly, 1997; Wilson et al., 2002; Bartkus et al., 2003; Guillot et al., 2012; Shahcheraghi et al., 2014; Kamachi et al., 2020; Yamaguchi et al., 2020; Koide et al., 2022).
The earliest study on the drug resistance of BP in mainland of China was published in Jun 2008 (Ou, et al, 2008). In this study, 16 strains of BP were collected from 2000 to 2007 in Beijing and 4 strains were from 1970s. The results showed that all strains were ML-sensitive, and the MICs of ERY, AZM and CLA were very low. There were few studies on the resistance of BP in the following period in China, but combining the research conducted abroad of the same period (Korgenski and Daly, 1997; Wilson et al., 2002; Bartkus et al., 2003; Guillot et al., 2012);, we concluded that the incidence of ML-resistant BP was low in this period globally.
Then, in 2011, a cross-sectional study of BP seropositivity and carriage among healthy adolescents in Shandong Province, 2 ERY-resistant strains were identified with MIC>256μg/ml, and both clinical isolates had the A2047G mutation in the 23S rRNA (Zhang et al., 2013b). In 2012, 4 strains of ML-resistant BP were found in Xi’an, with A2047G mutation and all MICs of ERY, CLA and AZI were all >256ug/mL (Wang et al., 2013b). Several other studies have also shown that the molecular mechanism of ERY resistance is mainly related to the A2047G mutation in the V domain of 23S rRNA (Guillot et al., 2012; Wang et al., 2013b). A study in Xi’an (Wang et al., 2014) included 16 strains from 2012-2013, of which 87.5% (14/16) were resistant to ERY and all had A2047G mutation. Meanwhile, of the 100 samples positive for 23S rRNA PCR, 85 (85.0%) were found to have the A2047G mutation by sequencing. About the same time, data from Beijing showed that 91.9% (91/99) strains were resistant to MLs (MIC>256μg/ml), and all but one ERY-resistant strain contained the A2047G mutation (Yang et al., 2015b). Further studies conducted in Xi’an showed that the drug-resistant pertussis rate in Xi’an was 75.86-100% during 2012 to 2020, and the MIC50s of the involved bacteria to ERY, AZI and CLA were all >256μg/ml. However, some studies from south China such as Guangdong, Zhejiang, Hunan and Shanghai showed a relatively lower resistance rate (48.6%-77.1%) (Hua et al., 2019; Yan, 2019; Zhe et al., 2019; Zhang et al., 2020; Lin et al., 2022b), while it was generally higher in northern China (79.3%-100%) (Wang et al., 2014; Li et al., 2018; Li et al., 2019b; Li et al., 2019d; Juan et al., 2022).
Due to the high difficulty of pertussis culture, many regions do not carry out pertussis culture and susceptibility tests. Therefore, there is relatively little literature on pertussis resistance in China. Nevertheless, from the few studies at present, we can still see that the probability of BP resistant to MLs has increased significantly since 2010, although there are some regional differences. In order to overcome the difficulty of BP culture and avoid the missed diagnosis of drug-resistant BP, some studies also recommend the use of PCR-based sequencing for rapid detection of possible antimicrobial resistance (Wang et al., 2014; Zhang et al., 2017). Given that pertussis is clearly on the rise in China, concern about pertussis resistance is an ongoing and important issue.
Mycoplasma pneumoniae
MP is one of the main pathogens of CAP in children and adolescents. MLs are the main drugs for the treatment of MP infection. From 1968 to 1999, ML-resistant MP (MRMP) has been reported in only a few countries (Niitu et al., 1970; Stopler and Branski, 1986; Critchley et al., 2002; Pereyre et al., 2007). However, since 2000, the resistance rate has increased significantly and continuously (Okazaki et al., 2001; Morozumi et al., 2008).
The detection of drug resistance of MP started late in China but high rates of resistance were found at the outset. It was not until 2003 that Chinese scholars first reported that MP was 100% sensitive to AZM and roxithromycin (ROX), but all of them were resistant to ERY (Guo and Mai, 2003). To our knowledge, this is the first report of MRMP in China. In 2005, Xin reported (Xin et al., 2005) that 80% (4/5) of MP isolated in Beijing from 2003 to 2004 were resistant to ERY, ROX, CLA and AZM. Subsequently, they continued reported (Xin et al., 2006; Xin et al., 2009) the resistance rate of MLs was 69.2% (9/13) to 92% (46/50). The MICs of ERY, AZM and JOS were 512->1024μg/ml, 16-64 and 8-64 µg/mL, respectively. Meanwhile, they found all the drug-resistant strains were accompanied by 23S rRNA mutations, including A2063G (80%), A2063C (2%) and A2064G (10%) (Xin et al., 2009). Chen reported that the resistance rate to ERY in Hangzhou from 2006 to 2008 was 54.5-60.7% and it reached 78.9% (15/19) in 2009 (Chen et al., 2009). In a word, the MLs resistance of MP in China discovered late, but showed high resistance as soon as it was discovered.
Studies from 2010 onwards also showed high levels of resistance. Many studies showed that the resistance rate of MP to ERY in Beijing is relatively high and most of which were above 80% (Dong et al., 2013; Tian et al., 2013; Yin et al., 2013). Even in the study of 235 strains showed that the resistance rate of ERY reached 87% (Zhou et al., 2014b) in 2014. Similar trend was also found in other cities in Zhejiang province, and the drug resistance rate was relatively high (70.59%-100%) (Zhou et al., 2015; Chen et al., 2018; Lin et al., 2021). The study conducted in Guangdong showed that the resistance rate of ERY was 66.47-69.46% during 2014 to 2018. It’s relatively more sensitive to AZM (9.79%), ERY (5.34%), erythromycin istolate (1.59%), ROX (3.13%) and CLA (2.99%), but the resistance rate of JOS(36.44%) and acetylspiramycin (48.17%) to MP is higher (Chen et al., 2019). In subsequent reports, the resistant rate has gradually increased, fluctuating between 24% and 77% (Lu et al., 2020; Hung et al., 2021). According to the studies in other provinces and regions, the overall trend of MLs resistant MP in China is on the rise, but the reported resistance rate in Guangdong (5.34%), Yunnan (1.08%-5.64%) and Shanxi (64%) is lower than that in other regions (Ye et al., 2013; Chen et al., 2019; Jia et al., 2022; Lin et al., 2022c). In addition, some other studies conducted in Guangdong also showed that the rate of ERY in Guangdong (42.15-63%) was lower than that in Tianjin(92%), Shanghai (85.7%). (Liu et al., 2010; Xu et al., 2013; Ma et al., 2014; Du et al., 2017; Du et al., 2020). The distribution of MRMP is not even in the world. The resistance rate of MLs in East Asian countries represented by China is relatively high, while that in European and American countries is relatively low. Since the beginning of reporting, the drug resistance rate in Japan has shown an upward and then downward trend, where in 2009-2011, the rate was the highest at 72%. The reporting rate of European and American countries is relatively low, ranging from 0 to 27% (Wang et al., 2022).
Previous studies have revealed that there are 2 types of clinical isolates (type 1 and type 2), differing significantly in their P1 gene sequences (Su et al., 1990), and the resistance rate of type 2 isolates is relatively low (Zhao et al., 2012b; Xue et al., 2014; Shi et al., 2017; Qu et al., 2019). Before 2012, the epidemic strain in Beijing was type 1 for the P1 gene, and the genotype shift from type 1 to type 2 began in 2013 (Waites et al., 2008), which may explain the decrease in the proportion of MRMP in recent studies in Beijing. Several studies have shown that the A2063G mutation in the 23S rRNA gene domain V is the most common in MRMP isolates in China. In addition, A2064G, A2063C/T, C2617G/A, A430G, T279C, T508C, etc. are associated with the resistance (Zhang et al., 2014b; Jiang et al., 2021). A study in Zhejiang showed that (Zhou et al., 2015), A2063G channels are responsible for the inhibition of 14- and 15-member ring MLs (ERY MIC: 128->256μg/ml and AZM MIC: 32->64μg/ml, etc.), while retaining activity against 16-member ring MLs (JOS 1-8μg/ml).
From the current study, it can be seen that the incidence of MRMP is increasingly high in China, and only relatively low in a few areas. Although the drug resistance of MP cannot enhance the virulence of the pathogen, it will increase the difficulty of clinical treatment and limit the choice of antibiotics, and will cause more complications if the treatment is not timely (Zhou et al., 2014b). Therefore, it is necessary to continue to promote the monitoring of resistance.
Conclusion
In conclusion, various common pathogens such as SP, GAS, GBS, SA, BP and MP, have shown high resistance rates and high resistance level to MLs in Chinese children. The drug resistance of some pathogens occurs suddenly (such as MP and BP), which is a high drug resistance rate and high drug resistance level. There are regional differences in the resistance level of these pathogens. Mutations in the 23S rRNA site and/or carrying the ermB gene are currently common causes of resistance in these pathogens.
Author contributions
XM and LL contributed to conception and design of the study. JL, JG, HZ, XW and MX organized the database. LL and XM wrote the first draft of the manuscript. JL, HZ and JG wrote sections of the manuscript. All authors contributed to manuscript revision, read, and approved the submitted version.
Funding
This work was supported by grants from Key Laboratory of Pediatric Respiratory Disease in Jinan Children’s Hospital and Shandong Provincial Clinical Research Center for Children’s Health and Disease (SDPRC009).
Conflict of interest
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
The reviewer WZ declared a shared affiliation with the authors JL, HZ, JG to the handling editor at the time of review.
Publisher’s note
All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.
Supplementary material
The Supplementary Material for this article can be found online at: https://www.frontiersin.org/articles/10.3389/fcimb.2023.1181633/full#supplementary-material
References
Ardanuy, C., Domenech, A., Rolo, D., Calatayud, L., Tubau, F., Ayats, J., et al. (2010). Molecular characterization of macrolide- and multidrug-resistant Streptococcus pyogenes isolated from adult patients in Barcelona, Spain, (1993-2008). J. antimicrobial chemother 65 (4), 634–643. doi: 10.1093/jac/dkq006
Bao, J., Ye, L., Ma, Y., Song, S., Yang, J., Luo, Y., et al. (2021). Pathogenic spectrum of blood stream infections and realated drug resistance in a grade A territory hospital from 2018 to 2020 (in Chinese). Acad. J. Chin. PLA Med. School 42 (05), 525–532.
Bartkus, J. M., Juni, B. A., Ehresmann, K., Miller, C. A., Sanden, G. N., Cassiday, P. K., et al. (2003). Identification of a mutation associated with erythromycin resistance in Bordetella pertussis: implications for surveillance of antimicrobial resistance. J. Clin. Microbiol. 41 (3), 1167–1172. doi: 10.1128/jcm.41.3.1167-1172.2003
Berbel, D., Càmara, J., González-Díaz, A., Cubero, M., López de Egea, G., Martí, S., et al. (2021). Deciphering mobile genetic elements disseminating macrolide resistance in Streptococcus pyogenes over a 21 year period in Barcelona, Spain. J. antimicrobial chemother 76 (8), 1991–2003. doi: 10.1093/jac/dkab130
Bispo, P. J. M., Sahm, D. F., Asbell, P. A. (2022). A systematic review of multi-decade antibiotic resistance data for ocular bacterial pathogens in the United States. Ophthalmol. Ther. 11 (2), 503–520. doi: 10.1007/s40123-021-00449-9
Cao, Y., Wu, G., Guo, X. (1989). Maternal vaginal group B streptococcus investigation report (in Chinese). Modern Med. J. 03), 136–137+194.
Chang, H., Shen, X., Fu, Z., Liu, L., Shen, Y., Liu, X., et al. (2010). Antibiotic resistance and molecular analysis of Streptococcus pyogenes isolated from healthy schoolchildren in China. Scand. J. Infect. Dis. 42 (2), 84–89. doi: 10.3109/00365540903321598
Chen, R., Chen, Y., Black, S., Hao, C. L., Ding, Y. F., Zhang, T., et al. (2010b). Antibiotic resistance patterns and serotype distribution in Streptococcus pneumoniae from hospitalized pediatric patients with respiratory infections in Suzhou, China. J. Trop. Pediatr. 56 (3), 204–205. doi: 10.1093/tropej/fmp078
Chen, Y., Chen, R., Wu, Z., Lu, G. (2014b). Clinical analysis of 16 cases of neonatal early onset group B streptococcus sepsis (in Chinese). J. Pediatr. Pharm. 20 (11), 13–16. doi: 10.13407/j.cnki.jpp.1672-108X.2014.11.005
Chen, H., Deng, J., Ye, H., Long, Y., Chen, Y., Zhou, X. (2010a). Detection of erythromycin and tetracycine resistance-related genes in invasive inection due to group B streptococcus (in Chinese). Chin. J. Nosocomiol 20 (10), 1354–1357. doi: 10.1002/cjoc.20020201133
Chen, K., Huang, Y., Song, Q., Wu, C., Chen, X., Zeng, L. (2017). Drug-resistance dynamics of Staphylococcus aureus between 2008 and 2014 at a tertiary teaching hospital, Jiangxi Province, China. BMC Infect. Dis. 17 (1), 97. doi: 10.1186/s12879-016-2172-0
Chen, L.-l., Lin, M.-m., Shi, L.-f., Yu, J. (2018). Clinical correlation of Mycoplasma pneumoniae pneumonia in infants and youg children with 23S rRNA gene mutation of Mycoplasma pneumonia (in Chinese). Chin. J. Health Lab. Technol. 28 (12), 1434–1436.
Chen, X., Peng, Y., Bi, J., Yao, Z. (2014a). Detection of mecA gene in Staphylococcus aureus and its correlation with drug-resistance (in Chinese). Chongqing Med. 43 (11), 1312–1314.
Chen, Y., Sun, L., Ba, X., Jiang, S., Zhuang, H., Zhu, F., et al. (2022). Epidemiology, evolution and cryptic susceptibility of methicillin-resistant Staphylococcus aureus in China: a whole-genome-based survey. Clin. Microbiol. Infect. 28 (1), 85–92. doi: 10.1016/j.cmi.2021.05.024
Chen, C., Xu, H., Dan, Z., Yong, X., Pei, W., Li, D., et al. (2019). Surveillance of Mycoplasma pneuminiae antibiotic resistance in children from 2014 to 2018 (in Chinese). Chin. J. Nosocomiol 29 (12), 1850–1855. doi: 10.11816/cn.ni.2019-190832
Chen, M., Yao, W., Wang, X., Li, Y., Chen, M., Wang, G., et al. (2012). Outbreak of scarlet fever associated with emm12 type group A Streptococcus in 2011 in Shanghai, China. Pediatr. Infect. Dis. J. 31 (9), e158–e162. doi: 10.1097/INF.0b013e31825874f3
Chen, Y.-m., Zhang, W.-y., Yu, D.-j., Xiang, G.-q., Lu, Z., Wang, X.-j. (2009). Molecular mechanisms of macrolide resistance of mycoplasma pneumoniae (in Chinese). Chin. J. Nosocomiol 19 (08), 877–879+895. doi: 10.3321/j.issn:1005-4529.2009.08.003
Chi, J., Fu, Q., He, L., Luo, , Ren, X. J., Que, P., et al. (2018). Analysis of Staphylococcus aureus antimicrobial resistance in children form 2014 to 2017 (in Chinese). Chongqing Med. 47 (32), 4149–4152. doi: 10.3969/j.issn.1671-8348.2014.11.011
CHINET (2023) China Antimicrobial Surveillance Network (CHINET). Available at: http://www.chinets.com/Data (Accessed Jan. 2023).
Critchley, I. A., Jones, M. E., Heinze, P. D., Hubbard, D., Engler, H. D., Evangelista, A. T., et al. (2002). In vitro activity of levofloxacin against contemporary clinical isolates of Legionella pneumophila, Mycoplasma pneumoniae and Chlamydia pneumoniae from North America and Europe. Clin. Microbiol. Infect. 8 (4), 214–221. doi: 10.1046/j.1469-0691.2002.00392.x
De Azavedo, J. C., McGavin, M., Duncan, C., Low, D. E., McGeer, A. (2001). Prevalence and mechanisms of macrolide resistance in invasive and noninvasive group B streptococcus isolates from Ontario, Canada. Antimicrobial Agents chemother 45 (12), 3504–3508. doi: 10.1128/AAC.45.12.3504-3508.2001
Deng, Q., Deng, L., Xie, Y., Huang, Y., Zhong, H., Chen, J., et al. (2008). Distribution and drug resistance of impetigo pathogens in children (in Chinese). Guangdong Med. J. 05), 795–797. doi: 10.13820/j.cnki.gdyx.2008.05.015
Deng, J., Wan, Z., Mu, D., Zhou, W., Xiao, G., Xu, A., et al. (2012). Community-acquired Staphylococcus aureus and drug resistance test in healthy children in Chengdu (in Chinese). Modern Prev. Med. 39 (10), 2536–2538.
Deng, J., Zhu, J., Yang, C., Shu, M., Xiao, G., Su, M., et al. (2013). Clinical distribution and drug resistance of Staphylococcus aureus Isolated from hospitalized children (in Chinese). J. Sichuan Univ. (Medical Sciences) 44 (01), 159–161. doi: 10.13464/j.scuxbyxb.2013.01.006
Denis, O., Deplano, A., Nonhoff, C., De Ryck, R., de Mendonça, R., Rottiers, S., et al. (2004). National surveillance of methicillin-resistant Staphylococcus aureus in Belgian hospitals indicates rapid diversification of epidemic clones. Antimicrob. Agents Chemother. 48 (9), 3625–3629. doi: 10.1128/aac.48.9.3625-3629.2004
Ding, X., Li, M. (2022). Epidemiological study on Staphylococcus aureus (in Chinese). J. Pathogen Biol. 17 (12), 1442–1445. doi: 10.13350/j.cjpb.221216
Dong, X. P., Dong, Y. Q., Ma, L., Zhang, Z. H., Jiang, Y., Xin, D. L. (2013). Surveillance of drug-resistance in Mycoplasma pneumoniae and analysis of clinical features of Mycoplasma pneumoniae pneumonia in childhood. Chin. Med. J. (Engl) 126 (22), 4339. doi: 10.3760/cma.j.issn.0366-6999.20132405
Dong, T., Su, J., Huang, Z., Wei, H., Chen, J., Chen, Z., et al. (2001). Investigation of group A streptococcus carrier rate and drug resistance in children in Guangzhou (in Chinese). Chin. J. Lab. Med. 04), 39. doi: 10.3760/j:issn:1009-9158.2001.04.025
Dong, T., Su, J., Huang, Z., Wei, H., Chen, Y., Xu, L., et al. (1999). Study on group A streptococcus drug resistance in children in some areas of China (in Chinese). Chin. J. Pediatr. 01), 34–36. doi: 10.3760/j.issn:0578-1310.1999.01.011
Du, Q. (2022). The study of serotypes distribution and related resistance genes for group B streptococcus isolated from infant with invasive disease (in Chinese) (Master, Nanchang University).
Du, J.-l., Feng, Y., Li, H.-t. (2020). Role of real-time fluorescence quantitative PCR-binding probe in the determination of MP and MP drug resistance. Lab. Med. 35 (06), 535–539. doi: 10.3969/j.issn.1673-8640.2020.06.005
Du, D., Liao, S., Wu, Y., Jiao, Y., Wu, D., Wu, W., et al. (2017). Serological Analysis and Drug Resistance of Chlamydia pneumoniae and Mycoplasma pneumoniae in 4500 Healthy Subjects in Shenzhen, China. BioMed. Res. Int. 2017, 3120138. doi: 10.1155/2017/3120138
Du, Q. Q., Zeng, H. L., Yuan, L., Tang, P., Gao, W., Xu, J. J., et al. (2021). One cross-sectional investigation revealed that non-vaccine serotypes of Streptococcus pneumoniae could be identified more frequently in elderly Chinese people. Vaccine 39 (24), 3304–3309. doi: 10.1016/j.vaccine.2021.02.053
Duan, R., Peng, Y., Yu, X. (2000). Determination and drug resistance analysis of 382 strains of Staphylococcus in children blood culture (in Chinese). Jiangxi Med. J. 02), 103–104.
Fan, J., Yang, Y., Tong, Y., Ma, L. (2000). Methicillin-resistant Staphylococcus aureus in Beijing children's hospital,1993-1998 (in Chinese). Chin. J. Pediatr. 07, 38–40. doi: 10.3760/j.issn:0578-1310.2000.07.010
Farrell, D. J., Douthwaite, S., Morrissey, I., Bakker, S., Poehlsgaard, J., Jakobsen, L., et al. (2003). Macrolide resistance by ribosomal mutation in clinical isolates of Streptococcus pneumoniae from the PROTEKT 1999-2000 study. Antimicrob. Agents Chemother. 47 (6), 1777–1783. doi: 10.1128/aac.47.6.1777-1783.2003
Farrell, D. J., Morrissey, I., Bakker, S., Morris, L., Buckridge, S., Felmingham, D. (2004). Molecular epidemiology of multiresistant Streptococcus pneumoniae with both erm(B)- and mef(A)-mediated macrolide resistance. J. Clin. Microbiol. 42 (2), 764–768. doi: 10.1128/jcm.42.2.764-768.2004
Felmingham, D., Cantón, R., Jenkins, S. G. (2007). Regional trends in beta-lactam, macrolide, fluoroquinolone and telithromycin resistance among Streptococcus pneumoniae isolates 2001-2004. J. Infect. 55 (2), 111–118. doi: 10.1016/j.jinf.2007.04.006
Feng, L., Yang, Y., Yu, S., Yao, K., Yuan, L., Shen, X. (2010a). Antibiotic resistant pattern of group A beta-hemolytic streptococcus isolated from children (in Chinese). Chin. J. Infection Chemother 10 (02), 127–130. doi: 10.16718/j.1009-7708.2010.02.006
Feng, L., Yang, Y., Yu, S., Yao, K., Yuan, L., Shen, X. (2010b). Prevalence of fibronectin-binding protein in streptococcus pyogenes and its relationship with macrolide resistance (in Chinese). Chin. J. Infection Chemother 10 (01), 26–30. doi: 10.16718/j.1009-7708.2010.01.008
Francois Watkins, L. K., McGee, L., Schrag, S. J., Beall, B., Jain, J. H., Pondo, T., et al. (2019). Epidemiology of invasive group B streptococcal infections among nonpregnant adults in the United States 2008-2016. JAMA Internal Med. 179 (4), 479–488. doi: 10.1001/jamainternmed.2018.7269
Fu, P., Wang, C., Yu, H., Xu, H., Jing, C., Deng, J., et al. (2018). Antimicrobial resistance profile of clinical isolates in pediatric hospitals in China: report from the ISPED Surveillance Program,2017 (in Chinese). Chin. J. Evidence-Based Pediatr. 13 (06), 406–411. doi: 10.3969/j.issn.1673-5501.2018.06.002
Fu, P., Xu, H., Jing, C., Deng, J., Wang, H., Hua, C., et al. (2021). Bacterial epidemiology and antimicrobial resistance profiles in children reported by the ISPED program in China 2016 to 2020. Microbiol. Spectr. 9 (3), e0028321. doi: 10.1128/Spectrum.00283-21
Guillot, S., Descours, G., Gillet, Y., Etienne, J., Floret, D., Guiso, N. (2012). Macrolide-resistant Bordetella pertussis infection in newborn girl, France. Emerg. Infect. Dis. 18 (6), 966–968. doi: 10.3201/eid1806.120091
Guo, N., Mai, T. E. (2003). Pathogen detection and drug susceptibility analysis of pediatric pneumonia (in Chinese). Clin. J. Pract. Pediatr. 7), 542–543.
Guo, Y., Wang, M., Ma, L. (2000). Analysis of pathogenic bacteria and drug sensitivity in 430 cases of neonatal sepsis (in Chinese). Shaanxi Med. J. 07), 387–388.
Guo, Y., Zhang, F., Ni, K., Chu, X. (2012). Clinal distribution and drug susceptibilities of Streptococcus agalactiaes in hospital (in Chinese). Chin. J. Microecol 24 (11), 1016–1018. doi: 10.13381/j.cnki.cjm.2012.11.016
Han, R., Lv, F., Hou, A. (2007). Group A beta-hemolytic streptococcus drug resistance (in Chinese). Chin. J. Med. 08), 49–50. doi: 10.3969/j.issn.1008-1070.2007.08.017
He, X., Xie, M., Li, S., Ye, J., Peng, Q., Ma, Q., et al. (2017). Antimicrobial resistance in bacterial pathogens among hospitalized children with community acquired lower respiratory tract infections in Dongguan, China, (2011-2016). BMC Infect. Dis. 17 (1), 614. doi: 10.1186/s12879-017-2710-4
He, M., Yao, K., Shi, W., Gao, W., Yuan, L., Yu, S., et al. (2015). Dynamics of serotype 14 Streptococcus pneumoniae population causing acute respiratory infections among children in China, (1997-2012). BMC Infect. Dis. 15, 266. doi: 10.1186/s12879-015-1008-7
Hu, L., Li, Y., Lu, Y., Klena, J. D., Qiu, Y., Lin, Y., et al. (2016). Clinical characteristics, virulence factors and molecular typing of methicillin-resistant Staphylococcus aureus infections in Shenzhen City, China. Epidemiol. Infect. 144 (14), 3037–3045. doi: 10.1017/s0950268816001552
Hu, H., Xia, W. (2009). Drug-resistance of Staphylococcus aureus in children in Hubei during four years (in Chinese). Chin. J. Nosocomiol 19 (12), 1582–1583. doi: 10.3321/j.issn:1005-4529.2009.12.042
Hua, C., Li, J., Li, S. (2003). Antibiotics-resistant analysis of Staphylococcus aureus isolated from children in Hangzhou (in Chinese). Health Res. 05), 208–209+231.
Hua, C. Z., Wang, H. J., Zhang, Z., Tao, X. F., Li, J. P., Mi, Y. M., et al. (2019). In vitro activity and clinical efficacy of macrolides, cefoperazone-sulbactam and piperacillin/piperacillin-tazobactam against Bordetella pertussis and the clinical manifestations in pertussis patients due to these isolates: A single-centre study in Zhejiang Province, China. J. Glob Antimicrob. Resist. 18, 47–51. doi: 10.1016/j.jgar.2019.01.029
Huang, X., Chen, J. (2001). Analysis of bacterial resistance in children blood culture (in Chinese). Zhejiang Med. J. 04), 15–17.
Huang, C., Liu, X. (1990). Investigation on the changes of drug resistance of Escherichia coli and Staphylococcus aureus (in Chinese). Chongqing Med. 04), 36–37.
Huang, L., Liu, H., Huang, Y., Guan, X., Zhong, H., Xie, Y., et al. (2016). Susceptibility analysis of neonatal sepsis and meningitis group B streptococcus isolates in Guangzhou (in Chinese). Guangdong Med. J. 37 (12), 1873–1876. doi: 10.13820/j.cnki.gdyx.2016.12.029
Huang, S., Liu, X., Lao, W., Zeng, S., Liang, H., Zhong, R., et al. (2015b). Serotype distribution and antibiotic resistance of Streptococcus pneumoniae isolates collected at a Chinese hospital from 2011 to 2013. BMC Infect. Dis. 15, 312. doi: 10.1186/s12879-015-1042-5
Huang, X., Liu, Z., Shi, W. (2018). Analysis of 55 cases of early-onset GBS bloodstream infection in newborns (in Chinese). Chin. J. Perinatal Med. 21 (08), 531–536. doi: 10.3760/cma.j.issn.1007-9408.2018.08.005
Huang, J., Lu, X., He, X. (2014). Antibiotic resistance of clinical pathogenic bacteria distribution from 2010 to 2012 in the hospital (in Chinese). Heilongjiang Med. J. 38 (02), 154–158.
Huang, L., Xie, Y., Deng, Q., Liu, H., Zhong, H., Chen, Y., et al. (2015a). Analysis of antimicrobial resistance in 647 strains of Staphylococcus aureus isolated from pediatric patients (in Chinese). Chin. J. Infection Chemother 15 (02), 163–166. doi: 10.16718/j.1009-7708.2015.02.006
Hung, H., Chuang, C., Chen, Y., Liao, W., Li, S., Chang, I., et al. (2021). Clonal spread of macrolide-resistant Mycoplasma pneumoniae sequence type-3 and type-17 with recombination on non-P1 adhesin among children in Taiwan. Clin Microbiol Infect 27 (8), 1169.e1161–1169.e1166. doi: 10.1016/j.cmi.2020.09.035
Ikebe, T., Okuno, R., Kanda, Y., Sasaki, M., Yamaguchi, T., Otsuka, H., et al. (2021). Molecular characterization and antimicrobial resistance of group A streptococcus isolates in streptococcal toxic shock syndrome cases in Japan from 2013 to 2018. Int. J. Med. Microbiol. IJMM 311 (3), 151496. doi: 10.1016/j.ijmm.2021.151496
Ji, L., Yu, S., Liu, Y., Zhang, X., Gao, W., Ma, L., et al. (2012). The characteristrics of streptococcus pyogens from Chinese children with impetigo between 2003 and 2008 (in Chinese). Chin. J. Pract. Pediatr. 27 (06), 456–459.
Jia, H., Xu, J.-q., Li, F.-x., Hu, S.-h. (2022). Analysis of Distribution and Antibiotic Resistance of Mycoplasma pneumoniae infection in a hospital in Dali City from 2015 to 2020 (in Chinese). J. Dali Univ. 7 (08), 79–82. doi: 10.3969/j.issn.2096-2266.2022.08.017
Jiang, H., Kui, L., Huang, H., Su, M., Wen, B. (2013). Frequency distribution and antibiotic resistance of pathogens from the cerebrospinal fluid of 116 children with bacterial meningitis (in Chinese). Chin. J. Contemp. Pediatr. 15 (04), 264–267.
Jiang, F. C., Wang, R. F., Chen, P., Dong, L. Y., Wang, X., Song, Q., et al. (2021). Genotype and mutation patterns of macrolide resistance genes of Mycoplasma pneumoniae from children with pneumonia in Qingdao, China, in 2019. J. Glob Antimicrob. Resist. 27, 273–278. doi: 10.1016/j.jgar.2021.10.003
Jin, X., Li, M., Deng, W. (1999). Analysis on the pathogenic organisms isolated from lower respiratory tract of RICU patients and their drug resistence (in Chinese). Chin. J. Nosocomiol 04), 12–14.
Juan, Z., Di, Z., Chen, L., Ling, C., Chaofeng, M., Bao, C., et al. (2022). Comparison of macrolide resistance, molecular characteristics resistance and MAST types of Bordetella pertussis collected from Xi 'an and Shanghai (in Chinese). J. Xi'an Jiaotong Univ. (Medical Sciences) 43 (05), 691–696. doi: 10.7652/jdyxb202205010
Kamachi, K., Duong, H. T., Dang, A. D., Hai, T., Do, D., Koide, K., et al. (2020). Macrolide-resistant bordetella pertussis, Vietnam 2016-2017. Emerg. Infect. Dis. 26 (10), 2511–2513. doi: 10.3201/eid2610.201035
Koide, K., Yao, S., Chiang, C. S., Thuy, P. T. B., Nga, D. T. T., Huong, D. T., et al. (2022). Genotyping and macrolide-resistant mutation of Bordetella pertussis in East and South-East Asia. J. Glob Antimicrob. Resist. 31, 263–269. doi: 10.1016/j.jgar.2022.10.007
Korgenski, E. K., Daly, J. A. (1997). Surveillance and detection of erythromycin resistance in Bordetella pertussis isolates recovered from a pediatric population in the intermountain west region of the United States. J. Clin. Microbiol. 35 (11), 2989–2991. doi: 10.1128/jcm.35.11.2989-2991.1997
Lei, M., Zhang, Y., Guo, J. (2015). Clinical analysis of purulent meningitis related to streptococcus agalactiae in 22 newborns and infants (in Chinese). Chin. J. Pract. Pediatr. 30 (09), 696–700.
Lewis, K., Saubolle, M. A., Tenover, F. C., Rudinsky, M. F., Barbour, S. D., Cherry, J. D. (1995). Pertussis caused by an erythromycin-resistant strain of Bordetella pertussis. Pediatr. Infect. Dis. J. 14 (5), 388–391. doi: 10.1097/00006454-199505000-00010
Li, L., Deng, J., Ma, X., Zhou, K., Meng, Q., Yuan, L., et al. (2019b). High Prevalence of Macrolide-Resistant Bordetella pertussis and ptxP1 Genotype, Mainland China 2014-2016. Emerg. Infect. Dis. 25 (12), 2205–2214. doi: 10.3201/eid2512.181836
Li, S., Fu, L., Li, P., Wang, L. (2016). Analysis of drug resistance of Staphylococcus aureus from pediatric respiratory infection patients (in Chinese). Modern Prev. Med. 43 (06), 1023–1026.
Li, J., Gao, K., Rong, L., Guan, X., Deng, Q., Zhong, H., et al. (2018b). Resistance patterns and mechanism of group B streptococcus isolated from infants with invasive disease (in Chinese). Chin. J. Exp. Clin. Infect. Dis. (Electronic Edition) 12 (01), 20–27. doi: 10.3877/cma.j.issn.1674-1358.2018.01.005v
Li, J., Gao, K., Zeng, L., Zhu, S., Deng, Q., Hua, X., et al. (2018c). Clinical analysis and serotypes distribution of neonatal purulent meningitis caused by group B streptococcus (in Chinese). J. Pract. Med. 34 (04), 609–612. doi: 10.3877/cma.j.issn.1674-1358.2018.01.005
Li, J., Ji, W., Gao, K., Zhou, H., Zhang, L., Mu, X., et al. (2019a). Molecular characteristics of group B Streptococcus isolates from infants in southern mainland China. BMC Infect. Dis. 19 (1), 812. doi: 10.1186/s12879-019-4434-0
Li, J., Li, Y., Wang, J. (2003). Surveillance on gram-positive bacteria isolated from patients with hospital acquired infections or community acquired infections (in Chinese). Natl. Med. J. China 05), 16–25.
Li, L. J., Liu, Y., Jia, J., Yuan, L., Shi, W., Meng, Q. H., et al. (2019d). Antimicrobial susceptibility and antigen genotypes of Bordetella pertussis strains isolated from neonates (in Chinese). Zhongguo Dang Dai Er Ke Za Zhi 21 (3), 208–213. doi: 10.7499/j.issn.1008-8830.2019.03.004
Li, X., Wang, X., Hao, X., Wang, Q., Wang, J. (2020a). A multicenter study on clinical characteristics and drug sensitivity test of different invasive infection types of group B streptococci (in Chinese). Chin. J. Perinatal Med. 47 (20), 5–10. doi: 10.3760/cma.j.cn115689-20200507-02129
Li, L., Wang, F., Kong, C., Jin, P., Wu, L., Xie, H. (2019c). Analysis of pathogen distribution and drug resistance of 469 children with severe bacterial pneumonia in our hospital (in Chinese). China Modern Med. 26 (14), 117–120+127.
Li, G., Wang, Z., Shi, L. (2015). Investigation of nosocomial infection status and drug resistance of Streptococcus lactis in Huzhou Maternal and Children's Hospital (in Chinese). Chongqing Med. 44 (13), 1845–1847. doi: 10.3969/j.issn.1671-8348.2015.13.042
Li, R., Wang, J.A., Xu, J., Meng, X., Guan, Q., Sun, T., et al. (2012). Sputum bacteria culture and clinical analysis in 2097 infants with bronchiolitis (in Chinese). J. Shandong Med. Coll. 34 (06), 427–430.
Li, G., Wei, Z., Xu, S., Hai-tao, H., Yong, L. (2018). Analysis on drug resistance of Bordetella pertussis isolated in Tianjin (in Chinese). Dis. Surveillance 33 (07), 585–589. doi: 10.3784/j.issn.1003-9961.2018.07.012
Li, G., Xiong, J. (2001). Analysis of drug resistance of Pseudomonas aeruginosa and Staphylococcus aureus (in Chinese). Chin. J. Hosp. Pharm. 06), 35–36. doi: 10.3321/j.issn:1001-5213.2001.06.021
Li, J., Yang, Y., Yu, S., Yuan, L., Hu, Y. (1999). Antimicrobial resistance of Streptococcus pneumoniae (in Chinese). Chin. J. Pediatr. 07), 15–18. doi: 10.3760/j.issn:0578-1310.1999.07.005
Li, Q. H., Yao, K. H., Yu, S. J., Ma, X., He, M. M., Shi, W., et al. (2013). Spread of multidrug-resistant clonal complex 271 of serotype 19F Streptococcus pneumoniae in Beijing, China: characterization of serotype 19F. Epidemiol. Infect. 141 (12), 2492–2496. doi: 10.1017/s0950268813000514
Li, D., Zhang, S., Shi, Y., Li, X., Lu, B. (2018a). Antibiotic resistance and serotype distribution of group B streptococcus in pregnant women in Beijing (in Chinese). J. Capital Med. Univ. 39 (04), 591–595. doi: 10.3969/j.issn.1006-7795.2018.04.021 L986
Li, X., Zheng, F., Li, K. (2020b). Investigation and analysis of Class I integron of Staphylococcus aureus isolates in children and adults (in Chinese). Chin. J. Clin. Lab. Sci. 38 (09), 707–709. doi: 10.13602/j.cnki.jcls.2020.09.16
Liang, Z., Fu, J., Li, L., Yi, R., Xu, S., Chen, J., et al. (2021). Molecular epidemiology of Streptococcus pneumoniae isolated from pediatric community-acquired pneumonia in pre-conjugate vaccine era in Western China. Ann. Clin. Microbiol. Antimicrob. 20 (1), 4. doi: 10.1186/s12941-020-00410-x
Liang, Y., Shen, X., Huang, G., Wang, C., Shen, Y., Yang, Y. (2008). Characteristics of Streptococcus pyogenes strains isolated from Chinese children with scarlet fever. Acta Paediatr. 97 (12), 1681–1685. doi: 10.1111/j.1651-2227.2008.00983.x
Liang, T., Wang, D. (2019). ). Clinical features of sepsis caused by GBS infection in 60 infants (in Chinese). Maternal Child Health Care China 34 (22), 5213–5216. doi: 10.7620/zgfybj.j.issn.1001-4411.2019.22.44
Lin, Y., Chen, S., Xun, Z., Zhang, Z., Yan, X., Guo, S., et al. (2015). Clinical distributionsand drug resistance of 179 isolates of Streptococcus agalactiaes (in Chinese). Int. J. Lab. Med. 36 (10), 1376–1378.
Lin, W.-q., Mou, Y.-y., Xiang, J.-j., Cai, B.-b., Feng, J.-h. (2021). Detection of 23S rRNA gene in throat swabs and the diagnosis of drug-resistant Mycoplasma pneumoniae infection in children (in Chinese). Maternal Child Health Care China 36 (11), 2627–2630. doi: 10.19829/j.zgfybj.issn.1001-4411.2021.11.058
Lin, H., Shen, X., Yang, Y., Zheng, Y., Fu, Z. (2010). “"Changes in emm classification, drug resistance and resistance mechanism of clinical isolates of group A streptococcus in children in China" (in Chinese),” in The 15th National Pediatrics academic Conference of the Chinese Medical Association, 342.
Lin, W., Song-tao, B., Rui, H., Yu-qin, W., Li, T., Tao, Y., et al. (2022c). Macrolide-resistant Mycoplasma pneumoniae in children under 10 years old in Kunming (in Chinese). J. Clin. Pathological Res. 42 (05), 1080–1085. doi: 10.19829/j.zgfybj.issn.1001-4411.2021.11.058
Lin, F., Wu, J., Wang, Y., Chen, L., Zhang, Q. (2022a). Analysis and prevention of related causes of neonatal group B streptococcus infection (in Chinese). Heilongjiang Med. J. 46 (16), 1960–1962. doi: 10.3969/j.issn.1004-5775.2022.16.010
Lin, L. N., Zhou, J. S., Hua, C. Z., Bai, G. N., Mi, Y. M., Zhou, M. M. (2022b). Epidemiological and clinical characteristics of pertussis in children and their close contacts in households: A cross-sectional survey in Zhejiang Province, China. Front. Pediatr. 10. doi: 10.3389/fped.2022.976796
Lin, X., Zhu, Y., Lin, Y., Liu, D., Xu, L., Zhong, R., et al. (2019). A multicenter study on clinical characteristics and drug sensitivity test of different invasive infection types of group B streptococci (in Chinese). Chin. J. Perinatal Med. 08), 597–603. doi: 10.3760/cma.j.issn.1007-9408.2019.08.012
Liu, H., Chen, L., Li, L., Wang, Q., Zhou, M., Yang, L. (2019). Clinical analysis of 16 cases of neonatal sepsis caused by group B hemolytic streptococcus (in Chinese). Jiangxi Med. J. 54 (07), 803–805. doi: 10.3969/j.issn.1006-2238.2019.7.031
Liu, Z., Hu, B., Bi, Z., Kou, Z., Fang, M., Chen, B., et al. (2015). Antibiotic resistance on group A streptococcus among children in 4 cities of Shandong province in 2013 (in Chinese). J. Shandong University(Health Sciences) 53 (01), 77–80. doi: 10.6040/j.issn.1671-7554.0.2014.679
Liu, X., Ji, P., Jia, W., Wang, X., Wu, Z., Shan, B., et al. (2021b). A multicentric study on the distribution and the antibiotic sensitivity of major isolates in children infections from 2018 to 2020 (in Chinese). Chin. J. Antibiotics 46 (11), 1019–1025. doi: 10.13461/j.cnki.cja.007249
Liu, J., Liu, C., Zhang, Y., Yang, J., Jin, S., Li, F. (2021a). Clinal analysis of 54 cases of neonatal group B streptococcus septicemia (in Chinese). J. Wenzhou Med. Univ. 51 (04), 287–291. doi: 10.3969/j.issn.1004-5775.2022.16.010
Liu, X., Shen, X., Chang, H., Huang, G., Fu, Z., Zheng, Y., et al. (2009). High macrolide resistance in Streptococcus pyogenes strains isolated from children with pharyngitis in China. Pediatr. Pulmonol 44 (5), 436–441. doi: 10.1002/ppul.20976
Liu, Y., Wang, H., Chen, M., Sun, Z., Zhao, R., Zhang, L., et al. (2008). Serotype distribution and antimicrobial resistance patterns of Streptococcus pneumoniae isolated from children in China younger than 5 years. Diagn. Microbiol. Infect. Dis. 61 (3), 256–263. doi: 10.1016/j.diagmicrobio.2008.02.004
Liu, Y., Ye, X., Zhang, H., Xu, X., Li, W., Zhu, D., et al. (2010). Characterization of macrolide resistance in Mycoplasma pneumoniae isolated from children in Shanghai, China. Diagn. Microbiol. Infect. Dis. 67 (4), 355–358. doi: 10.1016/j.diagmicrobio.2010.03.004
Long, Y., Wang, Z. (2012). Analysis on the drug resistance of 106 Staphylococcus aureus from neonates (in Chinese). Modern Prev. Med. 39 (18), 4797–4798.
Lu, C. Y., Yen, T. Y., Chang, L. Y., Liau, Y. J., Liu, H. H., Huang, L. M. (2020). Multiple-locus variable-number tandem-repeat analysis (MLVA) of macrolide-susceptible and -resistant Mycoplasma pneumoniae in children in Taiwan. J. Formos Med. Assoc. 119 (10), 1539–1545. doi: 10.1016/j.jfma.2019.12.008
Lyu, S., Yao, K. H., Dong, F., Xu, B. P., Liu, G., Wang, Q., et al. (2016). Vaccine serotypes of streptococcus pneumoniae with high-level antibiotic resistance isolated more frequently seven years after the licensure of PCV7 in Beijing. Pediatr. Infect. Dis. J. 35 (3), 316–321. doi: 10.1097/inf.0000000000001000
Ma, F., Wu, X., Hua, C. (2007). Resistance to antibiotics against Staphylococcus aureus isolated from children and adults in Hangzhou (in Chinese). Chin. J. Nosocomiol 03), 331–333. doi: 10.3321/j.issn:1005-4529.2007.03.033
Ma, Y., Yang, Y., Liang, Y., Yu, S., Yuan, L., Shen, X. (2008). The drug resistance analysis of group A beta-hemolytic streptococci and the detection of macrolide-resistant gene (in Chinese). Chin. J. Infection Chemother 8 (05), 338–342. doi: 10.16718/j.1009-7708.2008.05.006
Ma, L., Zhao, P., Yang, Y., Yuan, L., Tong, Y. (2000). The study of microbiology and antibiotic susceptibility of bacterial strains isolated from patients with impetigo (in Chinese). Chin. J. Dermatol. 06), 15–17.
Ma, Z., Zheng, Y., Deng, J., Ma, X., Liu, H. (2014). Characterization of macrolide resistance of Mycoplasma pneumoniae in children in Shenzhen, China. Pediatr. Pulmonol 49 (7), 695–700. doi: 10.1002/ppul.22851
Min, L., Zhou, S., Liu, F., Ke, J., Zhou, Y., Xiong, L. (2019). Drug resistance analysis of 704 strains of Staphylococcus aureus from children patients in Jiangxi Province (in Chinese). Exp. Lab. Med. 37 (04), 652–654+658. doi: 10.3969/j.issn.1674-1129.2019.04.029
Montes, M., Tamayo, E., Mojica, C., García-Arenzana, J. M., Esnal, O., Pérez-Trallero, E. (2014). What causes decreased erythromycin resistance in Streptococcus pyogenes? Dynamics of four clones in a southern European region from 2005 to 2012. J. antimicrobial chemother 69 (6), 1474–1482. doi: 10.1093/jac/dku039
Morozumi, M., Iwata, S., Hasegawa, K., Chiba, N., Takayanagi, R., Matsubara, K., et al. (2008). Increased macrolide resistance of Mycoplasma pneumoniae in pediatric patients with community-acquired pneumonia. Antimicrob. Agents Chemother. 52 (1), 348–350. doi: 10.1128/aac.00779-07
Nanduri, S. A., Petit, S., Smelser, C., Apostol, M., Alden, N. B., Harrison, L. H., et al. (2019). Epidemiology of invasive early-onset and late-onset group B streptococcal disease in the United States 2006 to 2015: multistate laboratory and population-based surveillance. JAMA Pediatr. 173 (3), 224–233. doi: 10.1001/jamapediatrics.2018.4826
Nie, S., Cheng, Z., Wang, Q., Fan, F., Xiao, X., Lu, X. (2018). Epidemiological characteristics of group B streptococcus colonized in pregnant women in Shenzhen (in Chinese). Chin. J. Infection Control 17 (06), 522–526. doi: 10.3969/j.issn.1671-9638.2018.06.012
Niitu, Y., Hasegawa, S., Suetake, T., Kubota, H., Komatsu, S., Horikawa, M. (1970). Resistance of Mycoplasma pneumoniae to erythromycin and other antibiotics. J. Pediatr. 76 (3), 438–443. doi: 10.1016/s0022-3476(70)80485-1
Ning, H., Chen, M., Wu, M., Lu, S., Wang, P. (2014). Analysis on drug resistance of Staphylococcus aureus in skin and soft tissue infections in children (in Chinese). Chin. J. Nosocomiol 24 (23), 5778–5780. doi: 10.11816/cn.ni.2014-135142
Okazaki, N., Narita, M., Yamada, S., Izumikawa, K., Umetsu, M., Kenri, T., et al. (2001). Characteristics of macrolide-resistant Mycoplasma pneumoniae strains isolated from patients and induced with erythromycin in vitro. Microbiol. Immunol. 45 (8), 617–620. doi: 10.1111/j.1348-0421.2001.tb01293.x
Ou, J., Yuan, L., Yao, K., Shen, X., Yang, Y. (2008). Antimicrobial susceptibility testing of Bordetella pertussis: a surveillance study (in Chinese). J. Clin. Pediatr. 06), 483–485. doi: 10.3969/j.issn.1000-3606.2008.06.009
Pan, F., Han, L., Huang, W., Tang, J., Xiao, S., Wang, C., et al. (2015). Serotype distribution, antimicrobial susceptibility, and molecular epidemiology of streptococcus pneumoniae isolated from children in Shanghai, China. PloS one 10 (11), e0142892. doi: 10.1371/journal.pone.0142892
Pereyre, S., Charron, A., Renaudin, H., Bébéar, C., Bébéar, C. M. (2007). First report of macrolide-resistant strains and description of a novel nucleotide sequence variation in the P1 adhesin gene in Mycoplasma pneumoniae clinical strains isolated in France over 12 years. J. Clin. Microbiol. 45 (11), 3534–3539. doi: 10.1128/jcm.01345-07
Qu, J., Chen, S., Bao, F., Gu, L., Cao, B. (2019). Molecular characterization and analysis of Mycoplasma pneumoniae among patients of all ages with community-acquired pneumonia during an epidemic in China. Int. J. Infect. Dis. 83, 26–31. doi: 10.1016/j.ijid.2019.03.028
Qu, J., Shen, Y., Yi, S. (2022). Distribution and drug resistance analysis of pathogenic bacteria of neonatal bloodstream infection from 2014 to 2019 (in Chinese). Lab. Med. Clinic 19 (11), 1549–1554. doi: 10.3969/j.issn.1672-9455.2022.11.030
Ran, Q., Huang, X., Xu, H., Wang, M., Qiu, P. (2017). Analysis of drug resistance of Staphylococcus aureus in children with skin and soft tissue infections (in Chinese). Chin. J. Nosocomiol 27 (24), 5688–5691. doi: 10.11816/cn.ni.2017-171584
Sanders, E., Foster, M. T., Scott, D. (1968). Group A beta-hemolytic streptococci resistant to erythromycin and lincomycin. New Engl. J. Med. 278 (10), 538–540. doi: 10.1056/NEJM196803072781005
Schito, G. C., Debbia, E. A., Marchese, A. (2000). The evolving threat of antibiotic resistance in Europe: new data from the Alexander Project. J. Antimicrob. Chemother. 46 (Suppl T1), 3–9. doi: 10.1093/oxfordjournals.jac.a020891
Schito, G. C., Felmingham, D. (2005). Susceptibility of Streptococcus pneumoniae to penicillin, azithromycin and telithromycin (PROTEKT 1999-2003). Int. J. Antimicrob. Agents 26 (6), 479–485. doi: 10.1016/j.ijantimicag.2005.04.022
Shahcheraghi, F., Nakhost Lotfi, M., Nikbin, V. S., Shooraj, F., Azizian, R., Parzadeh, M., et al. (2014). The first macrolide-resistant bordetella pertussis strains isolated from Iranian patients. Jundishapur J. Microbiol. 7 (6), e10880. doi: 10.5812/jjm.10880
Shen, A. D., Zhang, G. R., Wang, Y. H., Yang, Y. H. (2005). Susceptibility patterns and mechanisms of macrolide resistance in group B streptococcus isolates. Zhonghua Er Ke Za Zhi 43 (9), 661–664. doi: 10.3760/cma.j.issn.0578-1310.2005.09.107
Shi, Z., Jian, C. (2010). The distribution of non-repeated strains and the antimicrobial resistance of Staphylococcus aureus Isolated from blood culture (in Chinese). J. Trop. Med. 10 (02), 177–180.
Shi, W. X., Wu, S. S., Gong, C., Li, A. H., Huang, F. (2017). The epidemiological characteristics and drug resistance of Mycoplasma pneumoniae in patients with community-acquired pneumonia during 2011-2015 in 5 sentinel hospitals in Beijing. Zhonghua Yu Fang Yi Xue Za Zhi 51 (9), 832–836. doi: 10.3760/cma.j.issn.0253-9624.2017.09.011
Stopler, T., Branski, D. (1986). Resistance of Mycoplasma pneumoniae to macrolides, lincomycin and streptogramin B. J. Antimicrob. Chemother. 18 (3), 359–364. doi: 10.1093/jac/18.3.359
Stylianopoulos, A., Kelly, N., Garland, S. (2002). Is penicillin and/or erythromycin resistance present in clinical isolates of group B streptococcus in our community? Aust. New Z. J. obstetrics gynaecol 42 (5), 543–544. doi: 10.1111/j.0004-8666.2002.00543.x
Su, C. J., Chavoya, A., Dallo, S. F., Baseman, J. B. (1990). Sequence divergency of the cytadhesin gene of Mycoplasma pneumoniae. Infect. Immun. 58 (8), 2669–2674. doi: 10.1128/iai.58.8.2669-2674.1990
Su, J., Dong, T., Chen, Z., Wu, H., Chen, J., Gong, S., et al. (2003). Study on the relationship between T type and antimicrobia resistance in group A streptococcus (in Chinese). Chin. J. Clin. Lab. Sci. 05), 265–266. doi: 10.13602/j.cnki.jcls.2003.05.005
Sun, W. (2011). Current status of Staphylococcus aureus causing neonatal nosocomial infection and analysis of drug resistance (in Chinese). Chin. J. Nosocomiol 21 (24), 5193–5195.
Sun, L., Xiao, Y., Huang, W., Lai, J., Lyu, J., Ye, B., et al. (2022). Prevalence and identification of antibiotic-resistant scarlet fever group A Streptococcus strains in some paediatric cases at Shenzhen, China. J. Glob Antimicrob. Resist. 30, 199–204. doi: 10.1016/j.jgar.2022.05.012
Tan, X., Liu, M., Yang, Y., Li, B., Kang, M. (2019). Epidemiological characteristics of scarlet fever in Guangdong Province 2005-2017 (in Chinese). Dis. Surveillance 34 (05), 411–416. doi: 10.3784/j.issn.1003-9961.2019.05.010
Tatara, K., Gotoh, K., Okumiya, K., Teramachi, M., Ishimoto, K., Tanaka, Y., et al. (2020). Molecular epidemiology, antimicrobial susceptibility, and characterization of fluoroquinolone non-susceptible Streptococcus pyogenes in Japan. J. infection chemother 26 (3), 280–284. doi: 10.1016/j.jiac.2019.10.004
Tian, X. J., Dong, Y. Q., Dong, X. P., Li, J. Y., Li, D., Jiang, Y., et al. (2013). P1 gene of Mycoplasma pneumoniae in clinical isolates collected in Beijing in 2010 and relationship between genotyping and macrolide resistance (in Chinese). Chin. Med. J. (Engl) 126 (20), 3944–3948. doi: 10.3760/cma.j.issn.0366-6999.20131643
Vázquez-Laslop, N., Mankin, A. S. (2018). How macrolide antibiotics work. Trends Biochem. Sci. 43 (9), 668–684. doi: 10.1016/j.tibs.2018.06.011
Wadilo, F., Hailemeskel, E., Kedir, K., El-Khatib, Z., Asogba, P. C., Seyoum, T., et al. (2023). Prevalence of Group B Streptococcus maternal colonization, serotype distribution, and antimicrobial resistance in Sub-Saharan Africa: A systematic review and meta-analysis. J. Global antimicrobial resistance 32, 134–144. doi: 10.1016/j.jgar.2023.02.004
Waites, K. B., Balish, M. F., Atkinson, T. P. (2008). New insights into the pathogenesis and detection of Mycoplasma pneumoniae infections. Future Microbiol. 3 (6), 635–648. doi: 10.2217/17460913.3.6.635
Wang, Y. (2013). Analysis of drug resistance of 152 strains of Staphylococcus aureus (in Chinese). Med. J. Natl. Defending Forces Northwest China 34 (04), 358–359. doi: 10.16021/j.cnki.1007-8622.2013.04.016
Wang, W., Cai, G., Zhong, Y., Zhou, Y. (2011b). Drug-resistance surveillance and analysis of the staphylococcus aureus infection of children under 5-year in Zhuhai area (in Chinese). Chin. J. Child Health Care 19 (07), 657–660.
Wang, C. Y., Chen, Y. H., Fang, C., Zhou, M. M., Xu, H. M., Jing, C. M., et al. (2019a). Antibiotic resistance profiles and multidrug resistance patterns of Streptococcus pneumoniae in pediatrics: A multicenter retrospective study in mainland China. Med. (Baltimore) 98 (24), e15942. doi: 10.1097/md.0000000000015942
Wang, Z., Cui, Z., Li, Y., Hou, T., Liu, X., Xi, Y., et al. (2014). High prevalence of erythromycin-resistant Bordetella pertussis in Xi'an, China. Clin. Microbiol. Infect. 20 (11), O825–O830. doi: 10.1111/1469-0691.12671
Wang, Z., Li, Y., Hou, T., Liu, X., Liu, Y., Yu, T., et al. (2013b). Appearance of macrolide-resistant Bordetella pertussis strains in China. Antimicrob. Agents Chemother. 57 (10), 5193–5194. doi: 10.1128/aac.01081-13
Wang, P., Ma, Z., Tong, J., Zhao, R., Shi, W., Yu, S., et al. (2015a). Serotype distribution, antimicrobial resistance, and molecular characterization of invasive group B Streptococcus isolates recovered from Chinese neonates. Int. J. Infect. Dis. 37, 115–118. doi: 10.1016/j.ijid.2015.06.019
Wang, L., Shen, X., Lu, Q., Wang, Y., Zeng, Q., Chen, Y., et al. (2008). Susceptibility surveillance of gram-positive bacteria to antibiotics among children in China : A study in Beijing, Shanghai, Guangzhou and Chongqing during the period of 2000-2006 (in Chinese). J. Capital Med. Univ. 05), 626–631. doi: 10.3969/j.issn.1006-7795.2008.05.021
Wang, H. B., Song, Y. Y., You, Y. H., Wang, H. W., Han, Q. H., Zhao, J. H., et al. (2013a). Molecular epidemiological analysis of group A Streptococci isolated from children in Chaoyang District of Beijing 2011: emm types, virulence factor genes and erythromycin resistant genes. BioMed. Environ. Sci. 26 (9), 782–784. doi: 10.3967/0895-3988.2013.09.012
Wang, P., Tong, J. J., Ma, X. H., Song, F. L., Fan, L., Guo, C. M., et al. (2015b). Serotypes, antibiotic susceptibilities, and multi-locus sequence type profiles of Streptococcus agalactiae isolates circulating in Beijing, China. PloS One 10 (3), e0120035. doi: 10.1371/journal.pone.0120035
Wang, C., Wang, A., Zhang, H., Li, W., Sun, Z., Jian, C., et al. (2010). CHINET 2009 surveillance of antibiotic in streptococcus spp in China (in Chinese). Chin. J. Infection Chemother 10 (06), 426–429. doi: 10.16718/j.1009-7708.2010.06.006
Wang, X., Wu, L., Cen, K., Tu, Q., Wang, Z. (2020). Screening of group B streptococcus in late pregnancy for the prevetion of neoatal early-onset infection (in Chinese). Zhejiang Med. J. 42 (17), 1871–1874+1880. doi: 10.12056/j.issn.1006-2785.2020.42.17.2020-353
Wang, G., Wu, P., Tang, R., Zhang, W. (2022). Global prevalence of resistance to macrolides in Mycoplasma pneumoniae: a systematic review and meta-analysis. J. Antimicrob. Chemother. 77 (9), 2353–2363. doi: 10.1093/jac/dkac170
Wang, Q., Yang, Y., Geng, W., Wu, D., Yuan, L., Yu, S., et al. (2011a). Study on drug-resistance and genetic types of methicillin-resistant Staphylococcus aureus isolated in children with pneumonia (in Chinese). Chin. J. Pract. Pediatr. 26 (03), 183–186.
Wang, N., Yuan, G., Du, X. (2018). Clinical analysis of 30 neonates with early invasive infection of group B streptococcus (in Chinese). J. Electrocardiogram (Electronic Edition) 7 (04), 132–133.
Wang, Y., Zhu, L., Kong, D., Gao, W., Yao, K., Dong, F., et al. (2019b). Multidrug-resistant B streptococcal genome sequence analysis (in Chinese). Military Med. Sci. 43 (01), 63–67. doi: 10.7644/j.issn.1674-9960.2019.01.012
Westh, H., Knudsen, A. M., Gottschau, A., Rosdahl, V. T. (1991). ). Evolution of Staphylococcus aureus resistance to erythromycin in Denmark 1959 to 1988: correlations between characteristics of erythromycin-resistant bacteraemia strains. J. Hosp Infect. 18 (1), 35–43. doi: 10.1016/0195-6701(91)90091-l
Wilson, K. E., Cassiday, P. K., Popovic, T., Sanden, G. N. (2002). Bordetella pertussis isolates with a heterogeneous phenotype for erythromycin resistance. J. Clin. Microbiol. 40 (8), 2942–2944. doi: 10.1128/JCM.40.8.2942-2944.2002
Wu, C., Chen, J., Chen, M. (2019). Clinical features and drug resistance analysis of infection in skin and soft tissue in hospitalized children caused by Staphylococcus aureus (in Chinese). Chin. J. Disinfection 36 (03), 215–217. doi: 10.11726/j.issn.1001-7658.2019.03.018
Wu, X., Jian, S., Wang, M., Huang, Z., Li, P. (2013). Analysis of pathogenic bacteria and the drug resistance in 23 cases of neonatal septicemia (in Chinese). Int. J. Lab. Med. 34 (16), 2087–2088. doi: 10.7644/j.issn.1674-9960.2019.01.012
Wu, J., Wu, J., Huang, G. (2013). Drug resistance of Staphylococcus aureus causing respiratory tract infections in children from 2009 to 2011 (in Chinese). Chin. J. Nosocomiol 23 (15), 3764–3766.
Wu, Q., Zeng, T., Wang, Q., Yang, P., Pu, X., Yao, K., et al. (2014). Macrolide resistance in group A beta haemolytic streptococcus isolated from children in China ermB is related to Tn916 transposons family (in Chinese). Int. J. Lab. Med. 24 (27), 18–23.
Xia, W., Chen, Y., Mei, Y., Wang, T., Liu, G., Gu, B., et al. (2012). Changing trend of antimicrobial resistance among pathogens isolated from lower respiratory tract at a university-affiliated hospital of China 2006-2010. J. Thorac. Dis. 4 (3), 284–291. doi: 10.3978/j.issn.2072-1439.2012.02.04
Xiao, P., Zhang, S., Fu, J., Liang, Z. (2021). Antibiotic resistance and genetic background of Staphylococcus aureus in pediatric intensive care unit (in Chinese). J. Guangxi Med. Univ. 38 (01), 138–143. doi: 10.16190/j.cnki.45-1211/r.2021.01.022
Xiao, Y., Wei, Z., Shen, P., Ji, J., Sun, Z., Yu, H., et al. (2015). Bacterial-resistance among outpatients of county hospitals in China: significant geographic distinctions and minor differences between central cities. Microbes Infec. 17(6), 417–425. doi: 10.1016/j.micinf.2015.02.001
Xie, A., Liu, H. (2020). Clinical features and risk factors of neonatal bloodstream infection caused by group B streptococcus (in Chinese). Exp. Lab. Med. 38 (02), 311–313. doi: 10.7644/j.issn.1674-9960.2019.01.012
Xin, D.-l., Han, X., Li, J., Wei, T.-l., Hou, A.-c. (2006). Analysis of macrolides-resistance of Mycoplasma pneumoniae (in Chinese). Chin. J. Pract. Pediatr. 08), 616–617. doi: 10.3969/j.issn.1005-2224.2006.08.022
Xin, D.-l., Hou, A.-c., Wei, T.-l., Li, J., Ma, H.-q. (2005). Analysis of macrolide-resistance of Mycoplasma pneumoniae (in Chinese). Chin. J. Pediatr. 03), 56. doi: 10.3760/j.issn:0578-1310.2005.03.016
Xin, D., Mi, Z., Han, X., Qin, L., Li, J., Wei, T., et al. (2009). Molecular mechanisms of macrolide resistance in clinical isolates of Mycoplasma pneumoniae from China. Antimicrob. Agents Chemother. 53 (5), 2158–2159. doi: 10.1128/aac.01563-08
Xiong, X., Liu, C., Sun, J., Wang, L., Xu, W., Li, J. (2012). Clinical characteristics and drug resistance of invasive pneumococcal disease in children under 5 years old (in Chinese). Chin. Pediatr. Emergency Med. 06), 599–602.
Xu, Q., Lin, S.-x., Guo, W., Hou, X.-j., Wang, W., Peng, L. (2013). Molecular detection and analysis of resistance in Mycoplasma pneumoniae in children hospitalized with pneumonia in Tianjin (in Chinese). Tianjin Med. J. 41 (03), 216–219. doi: 10.3969/j.issn.0253-9896.2013.03.007
Xu, Y., Shao, J. (2002). Changes of pathogenic bacteria in pediatric patients of septicemia and drug resistance there of in Zhejiang Children's Hospital 1991~2000 (in Chinese). Natl. Med. J. China 14), 12–15.
Xue, G., Wang, Q., Yan, C., Jeoffreys, N., Wang, L., Li, S., et al. (2014). Molecular characterizations of PCR-positive Mycoplasma pneumoniae specimens collected from Australia and China. J. Clin. Microbiol. 52 (5), 1478–1482. doi: 10.1128/jcm.03366-13
Xue, L., Yao, K., Xie, G., Zheng, Y., Wang, C., Shang, Y., et al. (2010). Serotype distribution and antimicrobial resistance of Streptococcus pneumoniae isolates that cause invasive disease among Chinese children. Clin. Infect. Dis. 50 (5), 741–744. doi: 10.1086/650534
Yamaguchi, T., Kawasaki, Y., Katsukawa, C., Kawahara, R., Kawatsu, K. (2020). The first report of macrolide-resistant bordetella pertussis isolation in Japan. Jpn J. Infect. Dis. 73 (5), 361–362. doi: 10.7883/yoken.JJID.2019.421
Yan, L. (2019). Clinical comparison of pertussis infected with macrolides-resistant or macrolides-sensitive Bordetella pertussis (in Chinese) (Master, Zunyi Medical University).
Yang, J., Li, Y., Gao, P. (2015a). Monitor and resistance analysis of group AB-hemolytic streptococcus and PFGE typing during 2012-2014 (in Chinese). Chin. J. Health Lab. Technol. 25 (20), 3583–3585.
Yang, Y., Lu, Q., Deng, L., Shen, X., Zhang, H., Zhou, H., et al. (2002b). Surveillance of antimicrobial susceptibility of S .pneumoniae and H .influenzae in children among four hospitals from 2000 to 2001 (in Chinese). Chin. J. Pediatr. 08), 16–21. doi: 10.3760/j.issn:0578-1310.2002.08.008
Yang, F., Xu, X. G., Yang, M. J., Zhang, Y. Y., Klugman, K. P., McGee, L. (2008). Antimicrobial susceptibility and molecular epidemiology of Streptococcus pneumoniae isolated from Shanghai, China. Int. J. Antimicrob. Agents 32 (5), 386–391. doi: 10.1016/j.ijantimicag.2008.05.004
Yang, M., Yang, Y., Alexander, D., Shen, A., Tong, Y., Shen, X., et al. (2002a). Erythromycin resistant genes in group B streptococcus (in Chinese). Chin. J. Pediatr. 08, 25–28. doi: 10.3760/j.issn:0578-1310.2002.08.010
Yang, Y., Yao, K., Ma, X., Shi, W., Yuan, L., Yang, Y. (2015b). Variation in bordetella pertussis susceptibility to erythromycin and virulence-related genotype changes in China, (1970-2014). PloS One 10 (9), e0138941. doi: 10.1371/journal.pone.0138941
Yao, K., Lu, Q., Deng, L., Yu, S., Zhang, H., Deng, Q., et al. (2005). Carrier rate of Streptococcus pneumoniae and susceptibility thereof to antimicrobial drugs among children in China: a surveillance study in Beijing, Shanghai, and Guangzhou 2000—2002 (in Chinese). Natl. Med. J. China 28, 1957–1961. doi: 10.3760/j:issn:0376-2491.2005.28.004
Ye, R., Du, Z., Sun, Y., Xiao, L., Ding, S. (1988). Study on drug sensitivity test of Streptococcus pneumoniae (in Chinese). Microbiol. China 02), 65–69. doi: 10.13344/j.microbiol.China.1988.02.007
Ye, Y., Li, S.-l., Jiang, P., Wang, Y., Yang, C. (2013). Analysis on Mycoplasma pneumoniae 23SrRNA gene mutation site and drug resistance phenotypes (in Chinese). Lab. Med. 28 (01), 11–16. doi: 10.3969/j.issn.1673-8640.2013.01.003
Yin, Y. D., Cao, B., Wang, H., Wang, R. T., Liu, Y. M., Gao, Y., et al. (2013). Survey of macrolide resistance in Mycoplasma pneumoniae in adult patients with community-acquired pneumonia in Beijing, China. Zhonghua Jie He He Hu Xi Za Zhi 36 (12), 954–958. doi: 10.3760/cma.j.issn.1001-0939.2013.12.022
Yin, J., Zhang, W., Yang, D., Li, L., Dong, X. (2018). Etiological characteristics of Streptococcus pyogenes isolated from children with scarlet fever in Tianjin from 2012 to 2016 (in Chinese). Chin. J. Prev. Med. 52 (10), 1045–1049. doi: 10.3760/cma.j.issn.0253-9624.2018.10.015
Yu, X., Hu, Y. (2018). Species and antimicrobial resistance of pathogens from blood culture of neonates for three consececutive years (in Chinese). Chin. J. Infection Control 17 (01), 56–59. doi: 10.3760/cma.j.issn.0253-9624.2018.10.015
Yu, S., Tong, Y., Yuan, L., Li, Y., Yang, Y. (2001). Surveillance of antimicrobial resistance of Streptococcus pneumoniae, (1997-2000) (in Chinese). Chin. J. Pediatr. 08, 47–48. doi: 10.3760/j.issn:0578-1310.2001.08.014
Yu, S., Wang, J., Li, J., Li, Y., Wang, X., CG, W., et al. (2000). Resistance, serotypes and "hidden resistant clones" of Streptococcus pneumoniae among children in Beijing (in Chinese). Chin. J. Pediatr. 07), 23–26. doi: 10.3760/j.issn:0578-1310.2000.07.006
Zhai, R., Li, Y., Sun, Y., Mei, X., Qiu, G. (2016). The distribution and drug resistance of pathogens causing nosocomia bloodstream infections during three consecutive years in a hospital (in Chinese). Chin. J. Exp. Clin. Infect. Diseases(Electronic Edition) 10 (01), 36–40.
Zhan, S., Miu, P., Sun, B., Cheng, F. (2018). Clinal ananlysis of neonatal sepsis caused by group B streptococcus (in Chinese). J. Youjiang Med. Univ. Nationalities 40 (05), 459–461+476. doi: 10.3969/j.issn.1001-5817.2018.05.016
Zhang, Y. J., Chen, Y. S., Wang, Z. W., Li, Y. Q., Wang, D. X., Shang, Y., et al. (2013c). Serological and molecular capsular typing, antibiotic susceptibility and multilocus sequence typing of Streptococcus pneumoniae isolates from invasive and non-invasive infections. Chin. Med. J. (Engl) 126 (12), 2296–2303. doi: 10.3760/cma.j.issn.0366-6999.20122925
Zhang, J., Dong, Y., Zhao, R., Zheng, Y. (2015a). Infants with group B Streptococcus infection: a retrospective of 35 cases (in Chinese). Chin. J. Pract. Pediatr. 30 (03), 215–218. doi: 10.7504/ek2015030615
Zhang, P., Huang, J.E, Chen, H. (2013a). Drug resistance of Staphylococcus aureus in neonatal umbilical cord secretions (in Chinese). Chongqing Med. 42 (21), 2527–2528. doi: 10.3969/j.issn.1671-8348.2013.21.033
Zhang, H., Jin, Z. (2013). Study on the nosocomial infection of Staphylococcus aureus and its drug-resistance in neonatal intensive care unit (in Chinese). Modern Prev. Med. 40 (14), 2619–2621.
Zhang, J., Li, F., Luan, Y., Liu, Y., Wang, Z. (2017). Establishment of AS-PCR assay for 23S rRNA site variation of Bordetella pertussis (in Chinese). Chin. J. Public Health 34 (06), 923–926. doi: 10.11847/zgggws1115872
Zhang, Q., Li, M., Wang, L., Xin, T., He, Q. (2013b). High-resolution melting analysis for the detection of two erythromycin-resistant Bordetella pertussis strains carried by healthy schoolchildren in China. Clin. Microbiol. Infect. 19 (6), E260–E262. doi: 10.1111/1469-0691.12161
Zhang, Q., Liu, J., Ma, J., Li, J., Chen, M., Ma, H. (1998). Change in drug resistance of staphylococcus aureus:Analysis of 1279 strains (in Chinese). J. Bengbu Med. Coll. 05), 72–73.
Zhang, G., Liu, R., Zhang, H., Li, Y., Zhang, D., Li, J., et al. (2014a). Clinical features of inhaled and blood-borne Staphylococcus aureus pneumonia and analysis of antibiotic resistance of the pathogen in children (in Chinese). Chin. J. Contemp. Pediatr. 16 (10), 979–983. doi: 10.7499/j.issn.1008-8830.2014.10.004
Zhang, H., Lu, Q., Li, W., Jiang, W., Wu, S. (2000). Determination of drug resistance in 90 strains of Streptococcus pneumoniae (in Chinese). Lab. Med. 05), 289–290. doi: 10.3969/j.issn.1673-8640.2000.05.013
Zhang, T., Wang, B., Wang, S.-q., Tang, Y.-p., Liu, M.-l., Peng, S.-m., et al. (2014b). Correlation between drug-resistance and clinical treatment of Mycoplasma pneumoniae (in Chinese). Chin. J. Obstetrics Gynecol Pediatrics(Electronic Edition) 10 (01), 29–40. doi: 10.3877/cma.j.issn.1673-5250.2014.01.008
Zhang, J. S., Wang, H. M., Yao, K. H., Liu, Y., Lei, Y. L., Deng, J. K., et al. (2020). Clinical characteristics, molecular epidemiology and antimicrobial susceptibility of pertussis among children in southern China. World J. Pediatr. 16 (2), 185–192. doi: 10.1007/s12519-019-00308-5
Zhang, Q., Yan, H., Zhang, F. (2018). Effect of group B streptococcus (GBS) infection in late pregnancy on pregnancy outcomes (in Chinese). Hebei Med. 24 (04), 608–612. doi: 10.3969/j.issn.1006-6233.2018.04.021
Zhang, L., Yang, W., Zhang, L., Guo, Z., Chen, J., He, Q., et al. (2015b). Prevalence and antibiotic resistance of group B streptococcus isolated from perinatel pregnant women during the perid from 2009 to 2014 in Dongguan, Guangdong Province (in Chinese). Chin. J. Infection Chemother 15 (06), 575–578. doi: 10.16718/j.1009-7708.2015.06.013
Zhang, J., Yuan, L., Yang, Y., Wu, G., Yu, S., Qin, Y., et al. (1995). A study of Group B streptococcus carriers in 600 healthy pregnant women and their newborns (in Chinese). Chin. J. Epidemiol. 01), 36–39. doi: 10.3760/cma.j.issn.0254-6450.1995.01.116
Zhao, X., Jin, D., Zhu, Y. (2020). The comparison of clinical features and drug resistance between MRSA and MSSA infections in children (in Chinese). Anhui Med. Pharm. J. 24 (09), 1846–1849. doi: 10.3969/j.issn.1009-6469.2020.09.039
Zhao, C., Li, Z., Zhang, F., Zhang, X., Ji, P., Zeng, J., et al. (2017). Serotype distribution and antibiotic resistance of Streptococcus pneumoniae isolates from 17 Chinese cities from 2011 to 2016. BMC Infect. Dis. 17 (1), 804. doi: 10.1186/s12879-017-2880-0
Zhao, F., Lv, M., Tao, X., Huang, H., Zhang, B., Zhang, Z., et al. (2012b). Antibiotic sensitivity of 40 Mycoplasma pneumoniae isolates and molecular analysis of macrolide-resistant isolates from Beijing, China. Antimicrob. Agents Chemother. 56 (2), 1108–1109. doi: 10.1128/aac.05627-11
Zhao, C., Sun, H., Wang, H., Liu, Y., Hu, B., Yu, Y., et al. (2012a). Antimicrobial resistance trends among 5608 clinical Gram-positive isolates in China: results from the Gram-Positive Cocci Resistance Surveillance program, (2005-2010). Diagn. Microbiol. Infect. Dis. 73 (2), 174–181. doi: 10.1016/j.diagmicrobio.2012.03.003
Zhao, J., Wang, X., Liu, J. (2007). Infection and drug susceptibility analysis of Group B Streptococcus agalactiae (in Chinese). Chin. J. Lab. Diagnosis 11), 1545–1546. doi: 10.3969/j.issn.1007-4287.2007.11.049
Zhe, Z., Chun-zhen, H., Hong-jiao, W., Gao-liang, W., Yong-ping, X., Jian-ping, L., et al. (2019). “Clinical characteristics and in vitro drug resistance analysis of Bordetella pertussis infection in children,” in : Collection of papers from the academic conference of Zhejiang Medical Association Medical Microbiology and Immunology Branch in 2019, 95–96.
Zheng, G., Song, X., Huang, C., Ma, X. (2009). Antibiotics susceptibility analysis of sixty-two clinical Streptococcus pneumoniae Isolates (in Chinese). Chin. J. Nosocomiol 19 (15), 2031–2033. doi: 10.3321/j.issn:1005-4529.2009.15.045
Zhong, H., Guan, X., Xie, Y., Huang, L., Wu, X. (2015). Distribution of serotypes and drug sensitivity analysis of group B streptococcus among infants in Guangzhou area (in Chinese). Maternal Child Health Care China 30 (35), 6261–6263. doi: 10.7620/zgfybj.j.issn.1001-4411.2015.35.39
Zhou, H. (1997). Investigation and drug sensitivity test of methicillin-resistant Staphylococcus aureus (in Chinese). Guangzhou Med. J. 02), 65+64.
Zhou, W., Jiang, Y. M., Wang, H. J., Kuang, L. H., Hu, Z. Q., Shi, H., et al. (2014a). Erythromycin-resistant genes in group A β-haemolytic Streptococci in Chengdu, Southwestern China. Indian J. Med. Microbiol. 32 (3), 290–293. doi: 10.4103/0255-0857.136568
Zhou, Z., Li, X., Chen, X., Luo, F., Pan, C., Zheng, X., et al. (2015). Macrolide-resistant Mycoplasma pneumoniae in adults in Zhejiang, China. Antimicrob. Agents Chemother. 59 (2), 1048–1051. doi: 10.1128/aac.04308-14
Zhou, L., Tang, X., Fu, J. (2022). Antibiotic resistance and genetic background of Staphylococcus aureus in children with acute otitis media (in Chinese). J. Audiology Speech Pathol. 30 (01), 17–21. doi: 10.3969/j10.3969/j.issn.1006-7299.2022.01.004
Zhou, M., Wang, Z., Zhang, L., Kudinha, T., An, H., Qian, C., et al. (2021). Serotype distribution, antimicrobial susceptibility, multilocus sequencing type and virulence of invasive streptococcus pneumoniae in China: A six-year multicenter study. Front. Microbiol. 12. doi: 10.3389/fmicb.2021.798750
Zhou, Y., Zhang, Y., Sheng, Y., Zhang, L., Shen, Z., Chen, Z. (2014b). More complications occur in macrolide-resistant than in macrolide-sensitive Mycoplasma pneumoniae pneumonia. Antimicrob. Agents Chemother. 58 (2), 1034–1038. doi: 10.1128/aac.01806-13
Keywords: resistance, macrolides, bacteria, child, China
Citation: Li J, Liu L, Zhang H, Guo J, Wei X, Xue M and Ma X (2023) Severe problem of macrolides resistance to common pathogens in China. Front. Cell. Infect. Microbiol. 13:1181633. doi: 10.3389/fcimb.2023.1181633
Received: 07 March 2023; Accepted: 18 July 2023;
Published: 10 August 2023.
Edited by:
Yonghong Yang, Capital Medical University, ChinaCopyright © 2023 Li, Liu, Zhang, Guo, Wei, Xue and Ma. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
*Correspondence: Xiang Ma, bWF4aWFuZzAxNzZAMTYzLmNvbQ==; MjAyMDU4MDUwMDAyQGVtYWlsLnNkdS5lZHUuY24=
†These authors have contributed equally to this work