Figures
Abstract
Background
Sufficient details have not been specified for the epidemiological characteristics of Staphylococcus aureus (S. aureus) and methicillin-resistant Staphylococcus aureus (MRSA) among surgical site infections (SSIs) in mainland China. This systematic review aimed to estimate proportions of S. aureus and MRSA in SSIs through available published studies.
Methods
PubMed, Embase and four Chinese electronic databases were searched to identify relevant primary studies published between 2007 and 2012. Meta-analysis was conducted on the basis of logit-transformed metric for proportions of S. aureus and MRSA, followed by pre-defined subgroup meta-analysis. Random-effects meta-regression was also conducted to explore the impact of possible factors on S. aureus proportions.
Results
106 studies were included, of which 38 studies involved MRSA. S. aureus accounted for 19.1% (95%CI 17.2-21.0%; I2 = 84.1%) of all isolates in SSIs, which was roughly parallel to 18.5% in the United States (US) (P-value = 0.57) but significantly exceeded those calculated through the surveillance system in China (P-value<0.001). In subgroup analysis, S. aureus in patients with thoracic surgery (41.1%, 95%CI 26.3-57.7%; I2 = 74.4%) was more common than in those with gynecologic surgery (20.1%, 95%CI 15.6-25.6%; I2 = 33.0%) or abdominal surgery (13.8%, 95%CI 10.3-18.4%; I2 = 70.0%). Similar results were found in meta-regression. MRSA accounted for 41.3% (95%CI 36.5-46.3%; I2 = 64.6%) of S. aureus, significantly lower than that in the US (P-value = 0.001). MRSA was sensitive to vancomycin (522/522) and linezolid (93/94), while 79.9% (95%CI 67.4-88.4%; I2 = 0%) and 92.0% (95%CI 80.2-97.0%; I2 = 0%) of MRSA was resistant to clindamycin and erythromycin respectively.
Conclusion
The overall proportion of S. aureus among SSIs in China was similar to that in the US but seemed higher than those reported through the Chinese national surveillance system. Proportions of S. aureus SSIs may vary with different surgery types. Commonly seen in SSIs, MRSA tended to be highly sensitive to vancomycin and linezolid but mostly resistant to clindamycin and erythromycin.
Citation: Yang Z, Wang J, Wang W, Zhang Y, Han L, Zhang Y, et al. (2015) Proportions of Staphylococcus aureus and Methicillin-Resistant Staphylococcus aureus in Patients with Surgical Site Infections in Mainland China: A Systematic Review and Meta-Analysis. PLoS ONE 10(1): e0116079. https://doi.org/10.1371/journal.pone.0116079
Academic Editor: Nicholas G. Reich, University of Massachusetts, UNITED STATES
Received: June 22, 2014; Accepted: December 1, 2014; Published: January 20, 2015
Copyright: © 2015 Yang et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited
Data Availability: All relevant data are within the paper and its Supporting Information files.
Funding: This project was funded by MedImmune LLC, Gaithersburg, MD, USA, and Special Fund for Health-scientific Research in the Public Interest: Research & application for the prevention & control of nosocomial infections caused by multi-drug resistant bacteria (201002021). The funders had no role in study design, literature search, data collection and analysis, decision to publish, or preparation of the manuscript.
Competing interests: This study was partly supported by MedImmune LLC, a wholly owned subsidiary of AstraZeneca, mainly for literature search and data collection. The funding was received directly by Peking University Health Science Center. None was paid individually to the researchers in this study for any employment or consultancy for the company. Antibiotics discussed in this review were not the patents of the company or its products in development or on market. There is no further relevant information about the conflicts of interest to declare. This does not alter the authors’ adherence to all the PLOS ONE policies on sharing data and materials, as detailed online in the guide for authors.
Introduction
It has been widely accepted that surgical site infections (SSIs) are an important component of all the nosocomial infection. Three types of SSIs are defined by the Centers for Disease Control and Prevention (CDC), including superficial, deep incisional SSIs and organ-space SSIs, depending on the sites and the extent of infection [1], among which superficial incisional SSIs are more common than the other two types [2]. In the United States (US) 2%–5% of patients undergoing surgeries develop SSIs of varying severity [3]. In studies from Europe, SSIs have a similar incidence, hovering at 3%–5% among patients undergoing surgery [4, 5]. SSIs are associated with increased morbidity and mortality rate [6]. In addition, patients with SSIs have a heavy economic burden in terms of extended length of stay and increased costs of treatment [7].
Various pathogens can contribute to SSIs, but significant concern has been raised for Staphylococcus aureus (S. aureus) and methicillin-resistant Staphylococcus aureus (MRSA). As the primary pathogen, S. aureus constitute approximately 20% of SSIs cases among hospitals according to the CDC [8]. From 1992 to 2002 the proportion of SSIs caused by S. aureus increased from 16.6% to 30.9%, during which time MRSA isolates increased from 9.2% to 49.3% [9]. The 90 days post-operative mortality was 6.7% and 20.7% for SSIs patients with methicillin-susceptible S. aureus (MSSA) and MRSA, respectively [10]. Compared with MSSA, the additional hospital charge associated with MRSA was at least $40,000 [10].
In China, the proportions of S. aureus in SSIs have been available from the Nosocomial Infection Surveillance System since 1990s; however, the system which covers a wide range of nosocomial infections is not specific to SSIs and the statistics reported from the system to date remain far from sufficient to describe the epidemiology of S. aureus or MRSA in SSIs across the country. Up to now, only three studies [11–13] have been published on the basis of this system, reporting the proportion of S. aureus in SSIs. According to the data from 79 hospitals in the system S. aureus accounted for 12.7% (377/2,971) between 1999 and 2001 [11] and 13.5% (515/3812) between 1999 and 2005 [12] among pathogens in SSIs. The proportions of S. aureus in patients with superficial incisional, deep incisional and organ-space infections were 14.1%, 12.8% and 7.4% respectively between 1999 and 2007 based on the data from 110 hospitals [13]. Furthermore, several limitations of the publications from this system existed. Firstly, the selected hospitals in the studies seemed unable to represent all the nationwide hospitals. The number of hospitals within the system had amounted to 134 in 2001 [14], but none of the studies involved all or a random sample of the hospitals to estimate the proportion of S. aureus in SSIs patients, which may introduce selection bias. Secondly, the exact data about the proportions of MRSA and the proportions of drug resistance of MRSA in SSIs, which should be the main concern from the perspective of clinical practice, are not accessible in the studies. In addition, this system only provided the overall proportion of S. aureus rather than proportions by year, region, hospital level, and surgery type, which are likely to have more significant impact on decision-making for clinical practice and public health.
Understanding the nationwide epidemiological situation of S. aureus and MRSA in SSIs is vital for policy makers and clinicians to develop appropriate preventive countermeasures. As the national data in China remain inadequate, this systematic review aimed to estimate the proportions of S. aureus and MRSA in SSIs, by summarizing and assessing the available observational studies in China published from 2007 to 2012, to provide further evidence.
Methods
Information sources and search strategy
We performed systematic search in six electronic databases, including PubMed, Embase (OVID), Chinese BioMedical Database (CBM), China National Knowledge Infrastructure (CNKI), VIP Chinese Science and Technique Journals Database, and Wanfang Database, to identify the relevant studies. Since the focus in the review was on the epidemiological characteristics of S. aureus and MRSA in SSIs during recent years, search was limited to the publication date from January 2007 to November 2012. A combination of Mesh words and free text words applied to PubMed, Embase and CBM, and free text words were used to search CNKI, VIP and Wanfang database. The following search terms were mainly used: “surgery”, “wound infection*”, “postoperative wound infection*”, “surgical site infection*”, “S. aureus.”, “Staphylococcus aureus”, “methicillin”, “MSSA” and “MRSA”. Details of the search strategies for each database were summarized in S1 Table.
Eligibility criteria
Criteria of inclusion:
- Patients: those with SSIs regardless of other characteristics;
- Outcomes: S. aureus and MRSA isolates identified from SSIs;
- Study types: observational studies including cross-sectional, monitoring, prospective, ambispective and retrospective study.
Criteria of exclusion:
- Duplicate studies;
- Involvement of studied population from outside mainland China;
- Therapeutic study including randomized controlled trial and observational research for comparative effectiveness;
- Studies with data from the China Nosocomial Infection Surveillance System.
Study selection
According to the criteria of inclusion and exclusion, two reviewers independently screened each record by the title, keywords and abstract. The eligibility was determined further through the full texts if selection cannot be made only based on the screening. Any disagreement was resolved by the third reviewer.
Data extraction
An original extraction form was designed and then modified following a pilot test. The revised extraction form encompassed three parts: general information, clinical characteristics and numbers for calculating proportions of S. aureus and MRSA isolates. Two reviewers extracted information from each study independently. Any disagreement was also resolved by the third reviewer.
Assessment of risk of bias
As there were no acknowledged or standardized quality assessment tools for the included study designs, we used a checklist with 8 items adapted from a scale for case series [15], which was originally developed by the National Institute for Health and Care Excellence (NICE), a special health authority in the UK which is committed to providing national guidance and advice to improve health and social care. Low, high or unclear risk of bias for each item was determined according to the pre-specified criteria (S2 Table) and the graph of summary of risk of bias was developed with Revman 5.1. One point was scored if an item was judged low risk of bias. We defined study of higher quality with a total of at least 4 points.
Dealing with missing data
When information of the variables for analysis was missing from publications, the correspondent authors were contacted by email every one week. If the authors did not reply to the emails after our second contact attempt, the publications were excluded when the related variables were analyzed.
Statistical analysis
We conducted all the data analyses using R (Version 3.1.2, The R Foundation for Statistical Computing).
Calculation formula for the proportions of S. aureus and MRSA
Proportions of S. aureus and MRSA isolates were calculated by the following formula for each related study:
Incremental 0.5 was added to both the numerator and denominator in studies with zero or all events. 95% CI for the proportion in each study was calculated based on the logit-transformed metric.
Pooled overall proportions
Meta-analysis was conducted for the pooled estimates, followed by comparison between our overall estimate of S. aureus and MRSA and the corresponding proportions in the US and in the China Nosocomial Infection Surveillance System. Statistical difference between the proportions in such comparisons was tested by Q statistic for heterogeneity [16]. P-value of less than 0.05 indicated statistical significance. Considering probable heterogeneity across all the observational studies, random-effects model with Der-Simonian Laird method was used a priori throughout the data analyses.
Heterogeneity and subgroup analysis
Q test and I2 statistic were used to examine and quantify the heterogeneity of the logit-transformed proportion across the studies. P-value of less than 0.05 or I2 statistic of more than 50% were regarded as substantial heterogeneity [17]. Subgroup analysis was conducted to explore the possible sources of heterogeneity based on the pre-defined variables including study quality, sample size, region, level of hospital, provincial economic condition, types of surgeries. A map for the distribution of S. aureus was drawn through MapInfo Professional 11.0 according to the subgroup analysis by provinces. We determined small sample size if at most 20 bacteria isolates or S.aureus isolates were included in analysis for primary studies respectively reporting the proportion of S. aureus or MRSA. Based on whether the annual Gross Domestic Product (GDP) per capita of each province in 2011 was higher or lower than the national average (35,181RMB) in China, provinces were categorized into higher or lower provincial economic condition [18].
Informal comparisons were made between subgroups for the proportions of S. aureus and MRSA by directly comparing the magnitudes of proportions between different subgroups instead of significance tests which tend to be misleading for the comparison in subgroup analysis. Statistical significance was defined as non-overlap of the confidence intervals of the proportions between the subgroups [19].
Meta-regression for the proportion of S. aureus isolates
Meta-regression was used to explore the impact of pre-defined factors on the proportion of S. aureus isolates. We defined logit(P) as the dependent variable where P referred to proportion of S. aureus isolates. All the independent factors were initially selected based on the expertise in clinical microbiology and the availability of related information in the included articles, including study quality, sample size, region, level of hospital, provincial economic condition and type of surgery, all of which were defined as dummy variables. The factors without colinearity indicated by no correlation to each other (P-value≥0.10) were finally included into the random-effects meta-regression model with restricted maximum likelihood (REML) method. The statistical significance of any single coefficient was tested by Z-test and 0.05 was used as the threshold of P-value for statistically significant difference.
Publication bias
Egger’s test served to assess the probability of publication bias for the overall S. aureus and MRSA proportion [20]. The test was based on the logit-transformed proportion and corresponding standard error. A P-value of less than 0.10 was regarded as statistical significance, indicating probable publication bias.
Results
General information about included studies
We retrieved 2904 references from six databases, of which 106 studies were eligible for inclusion (Fig. 1). All the studies, 105 published in Chinese and one in English, were hospital-based. Table 1, Table 2 and S3 Table show detailed characteristics of included studies.
Methodological quality of studies
The methodological quality of studies was displayed in Fig. 2 with more details in S2 Table, S1 Fig The maximum score that studies achieved was 7 while the minimum was 0. We finally identified 38 studies with relatively high quality which reached at least 4 scores in our quality assessment scale.
Overall proportions
106 studies, including a total of 13,608 isolates, reported proportions of S. aureus isolates. The pooled proportion of S. aureus isolates among patients with SSIs was 19.1% (95%CI 17.2–21.0%; I2 = 84.1%) (Fig. 3). The proportion was similar to 18.5% (1,452/7,848, 95%CI 17.7–19.4%) (Q = 0.32, df = 1, P-value = 0.570) in the US, but significantly exceeded the proportions of 12.7% (377/2,971, 95%CI 11.5–13.9%) (Q = 33.4, df = 1, P-value<0.001) and 13.5% (515/3,812, 95%CI 12.5–14.6%) (Q = 28.3, df = 1, P-value<0.001) reported through the China Nosocomial Infection Surveillance System.
With respect to the proportion of MRSA, 1,502 isolates of S. aureus in 38 studies were included. The overall proportion of MRSA isolates was 41.3% (95%CI 36.5–46.3%; I2 = 64.6%) (Fig. 4). The proportion was significantly lower (Q = 10.3, df = 1, P-value = 0.001) than that of 53.9% in the US (150/278, 95%CI 48.1–59.7%).
No evidence in Egger’s test suggested publication bias for the overall proportion of S. aureus (t=-1.10, P-value = 0.275) and MRSA (t = 0.46, P-value = 0.651).
Subgroup analysis
All the results of subgroup analysis were summarized in Table 3 and the forest plots were presented in S1 File.
The pooled proportion was 41.1% (95%CI 26.3–57.7%; I2 = 74.4%) for thoracic surgeries, 20.4% (95%CI 15.3–26.7%; I2 = 87.8%) for orthopedics surgeries, 20.1% (95%CI 26.3–57.7%; I2 = 74.4%) for gynecologic surgeries and 13.8% (95%CI 10.3–18.4%; I2 = 70.0%) for abdominal surgeries. In addition, S. aureus proportion was higher in studies conducted in low economic condition, rural or non-tertiary hospitals or with small sample size (at most 20 isolates of bacteria), although significant differences between subgroups were not found. On the other hand, the proportions seemed similar in studies with high and low quality, those with retrospective and non-retrospective design, or those beginning before and since 2007 (Fig. A-I in S1 File).
Geographical differences in S. aureus proportions by different provinces or municipalities across China were shown in Fig. 5. Among 21 areas the maximum point estimate of S. aureus proportion among all the provinces with available data was 33.3% (95%CI 15.8–57.1%) in Ningxia province, followed by Tianjin municipality (30.2%, 95%CI 21.9–40.1%) and Jiangxi province (30.0%, 95%CI 16.9–47.4%) and the minimum was 11.5% (95%CI 8.1–16.1%) in Gansu province. However, there was only one study available, respectively, for the proportion estimate in Ningxia, Jiangxi and Gansu.
Regarding the pooled proportion of MRSA isolates (Fig. J-R in S1 File), the proportion was 55.0% (95%CI 21.4–84.5%, I2 = 74.1%) for abdominal surgeries, 41.0% (95%CI 23.5–61.1%, I2 = 0%) for gynecologic surgeries, 39.1% (95%CI 3.8–91.2%, I2 = 94.0%) for thoracic surgeries and 26.6% (95%CI 15.3–42.2%, I2 = 56.9%) for orthopedics surgeries. Furthermore, despite insignificant difference between subgroups, MRSA proportion tended to be higher in low economic condition, urban and tertiary hospitals as well as in studies with small sample size (at most 20 S. aureus isolates). Similar proportions can be found between studies with higher and lower quality, studies with retrospective and non-retrospective design, or studies with the start time of before 2007 and since 2007.
All the MRSA were sensitive to vancomycin (522/522) while only one isolate was resistant to linezolid (1/94). 79.9% (95%CI 67.4–88.4%; I2 = 0%) and 92.0% (95%CI 80.2–97.0%; I2 = 0%) of MRSA, respectively pooled from four and five studies, were resistant to clindamycin and erythromycin (Fig. S and Fig. T in S1 File).
Meta-regression for the proportion of S. aureus isolates
97 studies without any missing data were included for meta-regression to identify related potential factors for heterogeneity with statistical significance. As we found a significant correlation coefficient between levels of hospital and region (coefficient = 0.570, P-value<0.001), provincial economic condition and region (coefficient=-0.198, P-value = 0.052), the region variable was therefore excluded out of the pre-defined independent factors for the meta-regression (Table 4).
The meta-regression (residual I2 = 83.3%, adjusted R2 = 17.6%, P-value<0.001 in the test for the goodness of model fit) showed that compared with thoracic, S. aureus proportion was significantly lower in abdominal (OR = 0.224, 95%CI 0.105–0.477, P-value<0.001), gynecologic (OR = 0.254, 95%CI 0.114–0.565, P-value<0.001) and orthopedic (OR = 0.352, 95%CI 0.171–0.726, P-value = 0.005) surgeries. Studies with relatively large sample size (>20 isolates) were likely to conclude lower proportions of S. aureus (OR = 0.582, 95%CI 0.344–0.985, P-value = 0.044).
Discussion
Proportions of S. aureus
The overall proportion of S. aureus isolates (19.1%) was consistent with the reported proportion of 18.5% in the US in 2003 [21], but was significantly higher than both estimated in the China Nosocomial Infection Surveillance System (12.7% between 1999 and 2001, 13.5% between 1999 and 2005) [11, 12]. This difference between our review and the Chinese surveillance system could not be attributed to the change over time because of insignificant difference between the studies starting before 2007 and those starting after 2007 by subgroup analysis. However, the following reasons may result in such difference. First, the surveillance result derived from only 79 of 134 surveillance hospitals (58.9%), which may reduce the representativeness of the practical situation in China. Nevertheless, 106 studies in our review involved more than 125 hospitals distributed in 21 different provinces or municipalities, including tertiary and non-tertiary hospitals, urban and rural areas, which may be more representative of the real national status. Second, the sample size of bacteria isolates from the surveillance system (only 3,812 in total) was substantially less than that included in our review (13,608). Pooling data from 106 studies with a larger sample size may provide a more reliable estimate for national situation.
In addition, our finding can provide further useful information which was not available from the Chinese surveillance system, such as the stratified proportions by the surgery type, economics condition, hospital level and province. As shown in the subgroup analysis, S. aureus proportions varied between different surgery types—highest for thoracic surgeries (41.1%) whereas lowest for abdominal surgeries (13.8%). Meta-regression suggested the similar result that patients undergoing thoracic surgeries were much more vulnerable to SSIs by S. aureus, compared with patients with any other involved surgery type. This result was consistent with the guideline for prevention of SSIs, which concluded that S. aureus was the dominant pathogen causing SSIs following thoracic surgeries [8], indicating that S. aureus should be highly suspected in the case of SSIs after thoracic surgeries. On the contrary, with other influencing factors adjusted, patients with abdominal surgeries were less likely to suffer from SSIs by S. aureus. Priority may not be given to S. aureus in the SSIs after this surgery type because gram-negative bacilli, rather than S. aureus, tend to be predominant in the gastrointestinal tract usually involved in abdominal surgeries [22, 23]. Impoverished regions, non-tertiary hospitals, and some provinces or municipalities such as Ningxia, Tianjin and Jiangxi, may also require more attention paid to S. aureus SSIs.
Proportions of MRSA
Our estimate focused on SSIs and thus may close the gap of the surveillance system in China which merely reported the MRSA proportion of 79.9% (3,177/3,975) in all kinds of hospital infections instead of in SSIs [12]. Comparison between the results indicated that the proportion of MRSA in SSIs may be lower than the average level among a diversity of hospital infections. Besides, our review concluded a significantly lower proportion than that reported in a recent multi-center study with a smaller sample size in the US [24]. However, the status quo necessitates further improvement since MRSA accounted for more than 40% of S. aureus in our review.
Variation in the MRSA proportions was found between different surgery types: highest in abdominal surgeries (55.0%) and lowest in orthopedics surgeries (26.6%). While a recent study showed cases with MRSA SSIs accounted for 30.4% in those with S. aureus SSIs in the US [22], the high MRSA proportion (55.0%) following abdominal surgeries in our study provided an alarming picture that, despite S. aureus being subordinate pathogen in SSIs after abdominal surgeries, physicians still have to be highly cautious about MRSA in SSIs. On the contrary, orthopedic surgeries saw the lowest proportion of MRSA SSIs (26.6%) in spite of its high proportion of S. aureus. A study also concluded that the proportion of MRSA was the lowest in orthopedic surgeries among all the surgical procedures, although the proportion (31.9%) they calculated was higher than ours [10]. However, the mechanism seems still unclear and requires further studies to confirm.
Proportions of antibiotic-resistant MRSA
Based on our findings, vancomycin and linezolid appeared to be still effective for treating MRSA in SSIs in vitro. Vancomycin therapy is the primary option in the case of limited current therapeutic methods for patients with MRSA infections [25]. In China, the surveillance system suggested that none of MRSA were resistant to vancomycin (0/3,102) between 1999 and 2005 in a variety of nosocomial infections including SSIs [12], which was similar to our result: we identified none of the MRSA isolates resistant to vancomycin (0/522) in SSIs. However, it is necessary to raise the awareness of the resistance of vancomycin since there has been evidence suggesting the observed rise in minimum inhibitory concentrations (MICs) of vancomycin from less than 0.5μg/mL in 2005 to 1.0 μg/mL in 2010 [26]. Linezolid is the first available oxazolidinone antibiotic, which uniquely inhibits bacterial protein synthesis by preventing formation of 70S initiation complex [27]. Although surveillance data on linezolid was absent, one of 94 MRSA isolates in our findings was resistant to linezolid. But currently no robust clinical evidence can demonstrate whether linezolid or vancomycin is superior in the treatment of MRSA SSIs [28]. Continuous surveillance of drug resistance for both antibiotics in this treatment is necessary and crucial for the clinical practice.
On the other hand, clindamycin and erythromycin, inhibiting protein synthesis by their effect on ribosome function and commonly used in clinical practice for MRSA SSIs [27, 29], may have a doubtful effectiveness. The proportion of MRSA resistant to clindamycin in our findings (79.9%) was also similarly suggested in the surveillance system for nosocomial infections—78.9% (1,137/1,445) [12]. In our review, more than 90.0% MRSA isolates were identified to be resistant to erythromycin, far higher than that in the UK bacteraemia surveillance where erythromycin resistance only occurred in 67% of MRSA [30]. As such, both treatments may not be the first choice when MRSA in SSIs is suspected.
Limitations
There are several limitations in this review. First, methodological quality of the included studies is the main concern for the combined estimates because less than half of the studies are of high quality according to our criteria. However, study quality seems not to be the main heterogeneity source as both subgroup analysis and meta-regression showed that the pooled result from studies of higher quality were consistent with that from those of lower quality. Second, we only included studies published after 2007 so as to understand the current proportion of S. aureus and MRSA in SSIs. Considering some studies had started before 2007, we conducted subgroup analysis for studies initiating before and after 2007 to ensure that it was reasonable to combine results from all included studies to provide more precise estimates and facilitate the meta-regression. Third, none of the pre-defined variables can fully explain the variance in proportions of S. aureus (I2 = 84.1%) and MRSA (I2 = 64.6%) in subgroup analysis and meta-regression, which could result in uncertainty around the pooled proportions. The major obstacle of extensively exploring the potential source of variation is the limited information about the heterogeneity reported in the publication, such as the duration of surveillance, MICs and molecular epidemiology, which may be significantly associated with the heterogeneity but cannot be examined in our review. However, meta-regression did find that some factors with available information, such as the types of surgery and sample sizes, may partly contribute to the heterogeneity across studies. In addition, despite informal comparisons between subgroups by 95%CI rather than the significance test, the problem with multiple comparisons may be raised in the comparisons with no adjustment made with a stricter criterion for the significant difference. Further study may also be required to confirm some pooled results derived from limited number of included studies in our review.
Conclusion
In conclusion, the overall proportion of S. aureus causing SSIs in mainland China was similar to that in the US, and the proportion of MRSA was possibly lower. The real proportion of S. aureus may be higher than that reported from the Chinese surveillance system. Both proportions of S. aureus and MRSA tended to depend on types of surgeries. Therefore, clinicians should take into account the types of surgery when taking care of post-operative patients and managing S. aureus and MRSA SSIs. Vancomycin and linezolid appeared to be effective for MRSA in SSIs. Further well-designed studies on this topic, including surveillance and primary prospective studies, are required to provide further reliable evidence.
Supporting Information
S2 Table. Quality assessment of the included studies.
https://doi.org/10.1371/journal.pone.0116079.s005
(DOCX)
S3 Table. Distribution of MRSA isolates resistant to specific antibiotics.
https://doi.org/10.1371/journal.pone.0116079.s006
(DOCX)
Author Contributions
Conceived and designed the experiments: ZY LH SZ. Performed the experiments: ZY JW WW Yuelun Zhang Yuan Zhang XN. Analyzed the data: ZY JW. Contributed reagents/materials/analysis tools: ZY JW WW Yuelun Zhang Yuan Zhang XN. Wrote the paper: ZY JW LH SZ.
References
- 1. Horan TC, Gaynes RP, Martone WJ, Jarvis WR, Emori TG (1992) CDC definitions of nosocomial surgical site infections, 1992: a modification of CDC definitions of surgical wound infections. Am J Infect Control 20: 271–274. pmid:1332552
- 2. Coello R, Charlett A, Wilson J, Ward V, Pearson A, et al. (2005) Adverse impact of surgical site infections in English hospitals. Journal of Hospital Infection 60: 93–103. pmid:15866006
- 3. Anderson D, Kaye K (2009) Staphylococcal surgical site infections. Infect Dis Clin North Am 23: 53–72. pmid:19135916
- 4. Astagneau P, Rioux C, Golliot F, Brücker G, INCISO Network Study Group (2001) Morbidity and mortality associated with surgical site infections: results from the 1997–1999 INCISO surveillance. J Hosp Infect 48: 267–274. pmid:11461127
- 5. Smyth E, McIlvenny G, Enstone J, Emmerson A, Humphreys H, et al. (2008) Four country healthcare associated infection prevalence survey 2006: overview of the results. J Hosp Infect 69: 230–248. pmid:18550218
- 6. Martone W, Nichols R (2001) Recognition, prevention, surveillance, and management of surgical site infections: introduction to the problem and symposium overview. Clin Infect Dis 33: S67–68. pmid:11486301
- 7. de Lissovoy G, Fraeman K, Hutchins V, Murphy D, Song D, et al. (2009) Surgical site infection: incidence and impact on hospital utilization and treatment costs. Am J Infect Control 37: 387–397. pmid:19398246
- 8. Mangram AJ, Horan TC, Pearson ML, Silver LC, Jarvis WR (1999) Guideline for prevention of surgical site infection, 1999. American Journal of Infection Control 27: 97–134. pmid:10196487
- 9. Jernigan J (2004) Is the burden of Staphylococcus aureus among patients with surgical-site infections growing? Infect Control Hosp Epidemiol 25: 457–460. pmid:15242191
- 10. Engemann JJ, Carmeli Y, Cosgrove SE, Fowler VG, Bronstein MZ, et al. (2003) Adverse clinical and economic outcomes attributable to methicillin resistance among patients with Staphylococcus aureus surgical site infection. Clin Infect Dis 36: 592–598. pmid:12594640
- 11. Wu A, Ren N, Wen X, Xu X, Li J (2005) Pathogens of surgical site infection. Zhonghua Yi Yuan Gan Ran Xue Za Zhi 15: 210–212.
- 12. Ren N, Wen X, Wu A (2007) Study on surveillance of drug resistance of Staphylococcus aureus in hospital infection in National Monitoring Net of Hospital Infection. Zhongguo Yi Xue Gong Cheng 5: 425–427.
- 13. Wen X, Ren N, Wu A, Xu X (2011) Distribution of pathogens causing nosocomial infection monitored by national nosocomial infection surveillance system and changing trend. Zhonghua Yi Yuan Gan Ran Za Zhi 21: 350–355.
- 14.
Wu A, Wen X, Ren N, Xu X, Yi X, et al. (2005) Pathogens causing nosocomial infection monitored by national nosocomial infection surveillance system and their change. Proceedings of the Twelfth Annual Academic Conference of the National Hospital Infection Management.
- 15.
National Collaborating Centre for Acute Care (2003) Preoperative tests: the use of routine preoperative tests for elective surgery. National Institute for Health and Clinical Excellence.
- 16.
Borenstein M, Hedges L, Higgins J, Rothstein H (2009) Introduction to Meta-analysis. Chichester (UK): John Wiley & Sons.
- 17. Higgins J, Thompson S, Deeks J, Altman D (2003) Measuring inconsistency in meta-analyses. BMJ 327: 557–560. pmid:12958120
- 18.
National Bureau of Statistics of China (2011) China Statistical Yearbook-2011. Beijing: China Statistics Press.
- 19.
Deeks J, Higgins J, Altman D (2011) Chapter 9: Analysing data and undertaking meta-analyses. In: Higgins J, Green S, editors. Cochrane Handbook for Systematic Reviews of Interventions Version 510 [updated March 2011]: The Cochrane Collaboration.
- 20. Egger M, Davey S, Schneider M, Minder C (1997) Bias in meta-analysis detected by a simple, graphical test. BMJ 315: 629–634. pmid:9310563
- 21. Gaynes R, Edwards J, National Nosocomial Infections Surveillance System (2005) Overview of nosocomial infections caused by gram-negative bacilli. Clin Infect Dis 41: 848–854. pmid:16107985
- 22. Ramirez MC, Marchessault M, Govednik-Horny C, Jupiter D, Papaconstantinou HT (2012) The Impact of MRSA Colonization on Surgical Site Infection Following Major Gastrointestinal Surgery. J Gastrointest Surg: 1–9.
- 23. Tlaskalová-Hogenová H, Stepánková R, Hudcovic T, Tucková L, Cukrowska B, et al. (2004) Commensal bacteria (normal microflora), mucosal immunity and chronic inflammatory and autoimmune diseases. Immunol Lett 93: 97–108. pmid:15158604
- 24. Anderson D, Kaye K, Chen L, Schmader K, Choi Y, et al. (2009) Clinical and financial outcomes due to methicillin resistant Staphylococcus aureus surgical site infection: a multi-center matched outcomes study. PLoS One 4: e8305. pmid:20016850
- 25. Stevens D, Herr D, Lampiris H, Hunt J, Batts D, et al. (2002) Linezolid versus vancomycin for the treatment of methicillin-resistant Staphylococcus aureus infections. Clin Infect Dis 34: 1481–1490. pmid:12015695
- 26. Zhao C, Sun H, Wang H, Liu Y, Hu B, et al. (2012) 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: 174–181. pmid:22521693
- 27. Santayana E, Jourjy J (2011) Treatment of methicillin-resistant Staphylococcus aureus surgical site infections. AACN Adv Crit Care 22: 5–12. pmid:21297385
- 28. Gurusamy K, Koti R, Toon C, Wilson P, Davidson B (2013) Antibiotic therapy for the treatment of methicillin-resistant Staphylococcus aureus (MRSA) infections in surgical wounds. Cochrane Database Syst Rev 8: CD009726. pmid:23963687
- 29. Weisblum B (1995) Erythromycin resistance by ribosome modification. Antimicrob Agents Chemother 39: 577–585. pmid:7793855
- 30. Gemmell CG, Edwards DI, Fraise AP, Gould FK, Ridgway GL, et al. (2006) Guidelines for the prophylaxis and treatment of methicillin-resistant Staphylococcus aureus (MRSA) infections in the UK. J Antimicrob Chemother 57: 589–608. pmid:16507559
- 31. Ao F, Wang B, Peng X, Liu X, Wang J, et al. (2007) Distribution and Drug Resistance of Pathogens from incisional infections after orthopedic surgery [in Chinese]. Gannan Yi Xue Yuan Xue Bao 27: 883–884, 896.
- 32. Chang F (2010) General Surgery-related Factors of Incision Infection and Interventions [in Chinese]. Zhonghua Yi Yuan Gan Ran Xue Za Zhi 20: 1674–1676.
- 33.
Chen B (2009) The analysis of the bacteria of the incisional infections in orthopedics operation in recent 3 years [in Chinese]. Chinese Nursing Care Association Conference of National Hospital Infections. pp. 50–54.
- 34. Chen H, Yang X, Fu X, Chen H, Deng Y (2009) Prospective study of the correlation between the time of draingage tube intubation after open cranial operation and the incidence of lacunar infection of intracranial organ [in Chinese]. Xian Dai Yi Yuan 9: 11–12.
- 35. Chen L, Zheng Y, Ma D (2010) Drug-resistance of Pathogens Isolated from Operative Incision [in Chinese]. Zhonghua Yi Yuan Gan Ran Xue Za Zhi 20: 419–420.
- 36. Chen X, Lin D, Lin H (2012) The surgical site infections of the pathogen research hospitals [in Chinese]. Zhongguo Yi Yao Zhi Nan 10: 4–5.
- 37. Cui Q, Li X, Ji S (2008) Investigation on incisional infection of 1001 cases after surgical operation in 2007 [in Chinese]. Yu Fang Yi Xue Lun Tan 14: 989–990.
- 38. Dai C (2012) Risk factors for incisional infections due to colorectal cancer surgery [in Chinese]. Zhonghua Yi Yuan Gan Ran Xue Za Zhi 22: 3532–3533.
- 39. Deng X, Zhang L, Liu Z, Ma L, Dou F (2010) Cross-sectional survey on surgical site infections in 10 hospitals [in Chinese]. Zhonghua Yi Yuan Gan Ran Xue Za Zhi 20: 1672–1673, 1682.
- 40. Ding H (2010) Investigation of the incisional infections in surgery [in Chinese]. Liaoning Yi Xue Za Zhi 24: 3.
- 41.
Dong Y (2007) The status and influence factors of patients’ infections after surgery [in Chinese]. Zhejiang: Zhejiang University. 51 p.
- 42. Duan Q, Chen H, Liu C (2008) The monitoring of bacterial drug resistance of incisional infections in the primary hospital [in Chinese]. Zhongguo Shi Yan Zhen Duan Xue 12: 1468–1469.
- 43. Fan W, Huang E, Duan L (2008) Distribution and drug resistance of pathogens in abdominal surgical wounds [in Chinese]. Zhonghua Yi Yuan Gan Ran Xue Za Zhi 18: 1562–1563.
- 44. Fan T, Hu H, Sun J (2010) Clinical observation of 36 cases with limb injury and incisional infections [in Chinese]. Zhongguo Yi Shi Jin Xiu Za Zhi 33: 30–32.
- 45.
Gu S, Mai W (2009) The analysis of 76 cases with incisional infectons on abdomen after caesarean section [in Chinese]. Zhongguo She Qu Yi Shi:.
- 46.
Hao M (2012) The anlysis and investigation of the bacteria in and after open fracture surgery [in Chinese]: Hebei Medical University. 32 p.
- 47. He Y (2012) The analysis and countermeasures of incisional infections in aseptic operations [in Chinese]. Nanchang Da Xue Xue Bao 52: 69–71.
- 48. Huang Y, Li L (2012) The anlysis of incisional infections after colorectal surgery (19 cases) [in Chinese]. Zhongguo Yi Yao Zhi Nan 10: 143–144.
- 49. Jiang Y, Kan Y, Wei W, Wei X (2009) The anlysis and preventive strategy of the bacteria in wound infections after open fractures surgery [in Chinese]. Zhejiang Lin Chuang Yi Xue 11: 390–392.
- 50. Jiang Y (2012) Targeted monitoring of incisional infections caused by cesarean section [in Chinese]. Zhonghua Yi Yuan Gan Ran Xue Za Zhi 22: 1391–1392.
- 51. Li D (2008) The clinical analysis of abdominal incisional infections after gynecologic surgery in 36 cases [in Chinese]. Zhongguo Shi Yong Yi Yao 3: 58–59.
- 52. Li D, Yang Y, Su H (2009) The surveillance of surgical site infections in a hospital in Neijiang [in Chinese]. Luzhou Yi Xue Yuan Xue Bao 32: 396–398.
- 53. Li L, Lin Z (2009) Clinical analysis of 15 cases with abdominal incisional infectons after caesarean section [in Chinese]. Zhongguo Dang Dai Yi Yao 16: 162–163.
- 54. Li M, Wei R (2009) An investigation of incisional infections after orthopedic aseptic operations in 14274 cases [in Chinese]. Zhong Yi Zheng Gu 21: 22–24.
- 55. Li Y (2010) Drug-resistance of pathogens from infected surgical wounds [in Chinese]. Zhonghua Yi Yuan Gan Ran Xue Za Zhi 20: 2338–2339.
- 56. Li Z, Shi W, Tan J (2010) Investigation on distribution and drug resistance of pathogenic bacteria in surgical incisional infections [in Chinese]. Shi Yong Yu Fang Yi Xue 17: 1430–1432.
- 57. Li X, Qin J, Feng Z, Gao W, Wang P (2010) Risk factors for surgical site infections in open fractures [in Chinese]. Zhonghua Yi Yuan Gan Ran Xue Za Zhi 20: 773–774.
- 58. Li H, Wei Y, Zheng P, Ling P, Li J (2011) Drug resistance of pathogens causing nosocomial infections [in Chinese]. Zhonghua Yi Yuan Gan Ran Xue Za Zhi 21: 2122–2123.
- 59. Li Y (2011) Clinic research about the cure of incision infection after gynecologic surgery [in Chinese]. An Mo Yu Kang Fu Yi Xue: 126–127.
- 60. Li X, Yang W (2012) The investigation and countermeasure of incisional infections after obstetric operations [in Chinese]. Zhongguo She Qu Yi Shi 14: 300.
- 61. Lin Z (2007) Analysis on common pathogens of surgical site infections and their drug resistance [in Chinese]. Zhi Ye Yu Jian Kang 23: 72–73.
- 62. Lin X, Zhan Y, Cai X (2008) Perioperative nursing care of aseptic incisional infections after orthopedics opertaions [in Chinese]. Guangdong Yi Xue 29: 1598–1599.
- 63. Lin S, Wu Y, Qiu L (2009) Investigation and analysis on risk factors for incisional wound infection after abdominal operations [in Chinese]. Yi Yao Shi Jie 11: 485–486.
- 64. Ling L, Zhang D (2011) Bacterial culture from wound secretion and drug susceptibility [in Chinese]. Zhonghua Yi Yuan Gan Ran Xue Za Zhi 21: 3044–3046.
- 65. Liu L, Wei Q, Zhang H, Zhong F, Su W (2008) Incisional infections after abdominal operations: investigation and strategy [in Chinese]. Zhonghua Yi Yuan Gan Ran Xue Za Zhi 18: 1091–1092.
- 66. Liu C, Cui X (2010) Analysis of incisional infections in 274 surgical cases [in Chinese]. Yi Yao Lun Tan Za Zhi 31: 116–117.
- 67. Liu W, Liu Y, Zhang N, Yan G (2011) Clinical analysis of orthopaedic sterile surgical incision infection and nursing countermeasures [in Chinese]. Zhonghua Yi Yuan Gan Ran Xue Za Zhi 21: 2689–2690.
- 68. Liu C, Zhao H, Hu J, Wen Y, Yang X (2012) The distribution and drug resistance of the pathogens in incisional infections after surgical treatment of breast cancer [in Chinese]. Jian Yan Yi Xue Yu Lin Chuang 9: 2167–2168.
- 69. Liu Z (2012) The analysis of 128 cases with incisional infections after abdominal operations [in Chinese]. Zhongguo Wei Sheng Chan Ye 9: 143–144.
- 70. Liu X, Zhang C (2012) Drug resistance of pathogenic bacteria causing surgical site infections and intervention countermeasures [in Chinese]. Zhonghua Yi Yuan Gan Ran Xue Za Zhi 22: 4385–4386.
- 71. Lv X, Huang J, Zhou P (2007) The study of distribution and antibacterial agents resistance of microorganism in general surgical site infections [in Chinese]. Zhongguo Wei Sheng Tai Xue Za Zhi 19: 213–214.
- 72. Lv S, Qu J, Xiang Y, Yang K, Jin C, et al. (2012) Pathogens causing surgical incisional infections afer colorectal cancer surgery and related factors [in Chinese]. Zhonghua Yi Yuan Gan Ran Xue Za Zhi 22: 4507–4508.
- 73. Mao G, Sun G (2011) Distribution and drug resistance of pathogens in patients with surgical incisional infections in orthotedics department [in Chinese]. Zhongguo Wei Sheng Jian Yan Za Zhi 21: 910–912.
- 74. Pang J (2007) The analysis of surgical incisional infections and antibiotic resistance [in Chinese]. Xi Bu Yi Xue 19: 85–86.
- 75.
Peng L, Chen X (2008) The analysis of the incisional infections in rural hospitals [in Chinese]. The Fifth Academic Conference of Analytic Microbiology Professional Committee of Hubei Microbiology Association. pp. 415–417.
- 76. Peng Y (2012) Distribution and risk factors of pathogenic bacteria causing surgical incisional infections [in Chinese]. Zhonghua Yi Yuan Gan Ran Xue Za Zhi 22: 840–842.
- 77. Peng Y, Chen X (2012) The analysis of drug resistance of the pathogens in surgical wound infections [in Chinese]. Zhongguo Wu Zhen Xue Za Zhi 12: 1618–1619.
- 78. Qian P, Li J, Ye J (2011) Pathogens causing perineal incisional infections and prevention measures [in Chinese]. Zhonghua Yi Yuan Gan Ran Xue Za Zhi 21: 819–820.
- 79.
Qu L, Zhang X (2008) The analysis of pathogenic bacteria in surgical incisional infections in primary level hospital [in Chinese]. The Third Academic Conference of National Bacteria Resistance Surveillance and Clinical Speciality pp. 519–520.
- 80. Qu C (2011) Investigation and intervention of incisional infections after surgeries [in Chinese]. Zhongguo Wei Sheng Chan Ye 8: 78.
- 81. Ren G, Hu F (2009) Pathogens distribution and drug sensitivity of the incisional infections: analysis of 23 cases [in Chinese]. Zhongguo She Qu Yi Shi 11: 181.
- 82. Ruan Y, Qin B, Guo L (2011) Factors associated with surgical site infections in patients with colorectal cancer [in Chinese]. Zhonghua Yi Yuan Gan Ran Xue Za Zhi 21: 2691–2693.
- 83. Sheng F (2012) Clinical characteristics of incisional infections after orthopedic surgeries and prevention measures [in Chinese]. Zhonghua Yi Yuan Gan Ran Xue Za Zhi 22: 4513–4514.
- 84. Shi W, Shi W, Li H (2011) Prospective surveillance on surgical site infections [in Chinese]. Zhongguo Gan Ran Kong zhi Za Zhi 10: 123–125.
- 85. Sun S, Liu M, Yang X (2008) Analysis of pathogens in postoperative infections on eyes [in Chinese]. Zhongguo Bing Yuan Sheng Wu Xue Za Zhi 3: 136–138.
- 86. Sun G, Shi L (2012) Distribution of pathogens causing surgical site infections and analysis of antimicrobial resistance [in Chinese]. Zhonghua Yi Yuan Gan Ran Xue Za Zhi 22: 843–844.
- 87. Tang M, Cui L, Shi D, Liang Y, Ma Q, et al. (2009) Central venous catheter related infections and risk factors after cardiovascular surgery [in Chinese]. Shan Xi Yi Xue Za Zhi 38: 47–49, 76.
- 88. Tang X, Xiao X, Chen S, Huang L, Tian W (2012) The cause of incisional infections, pathogens distribution and their drug sensitivity in 65 cases [in Chinese]. Guangdong Yi Xue Yuan Xue Bao 30: 411–412.
- 89. Tao G (2011) Neurological surgical site infections and countermeasures [in Chinese]. Zhonghua Yi Yuan Gan Ran Xue Za Zhi 21: 1544–1545.
- 90. Tian L, Shen J (2011) Investigation on antimicrobial resistance of pathogens from surgical incisions [in Chinese]. Lin Chuang Xue Ye Xue Za Zhi 24: 83–85.
- 91. Wan W, He Z, Zhang R, Wang J (2009) Distribution of pathogenic bacteria in surgical incisional infections and analysis of their antibiotics resistance [in Chinese]. Zhongguo Xian Dai Yi Sheng 47: 68–69, 71.
- 92. Wang A, Zhou J, Ma X, Dong L, Li G (2007) Surgical site infections after pancreas surgery and the use of perioperative antibiotics [in Chinese]. Zhongguo Yi Xue Ke Xue Yuan Xue Bao 29: 566–570. pmid:19209807
- 93.
Wang L (2007) The analysis of distribution and drug resistance of the pathogens in incisional infections [in Chinese]. Academic Conference of Environment and Health.
- 94. Wang Y, Wu D, Wang C (2008) The investigation about pathogens in open wounds in different time of doctors’ office visiting [in Chinese]. Zhonghua Yi Yuan Gan Ran Xue Za Zhi 18: 1783.
- 95. Wang X, Zhang Q, Chen J, Luo J (2012) Monitoring and analysis of postoperatice incisional infections in patients with gastrointestinal cancer [in Chinese]. Zhonghua Yi Yuan Gan Ran Xue Za Zhi 22: 2322–2324.
- 96. Wei L, Wen J, Li Z, Qiu Y (2010) Analysis on targeted surveillance data of incisional infections after cesarean section [in Chinese]. Zhongguo Fu You Bao Jian 25: 3395–3398.
- 97. Xiang D, Lian Y (2012) Analysis of risk factors and control measures for orthopedic sterile surgical wound infections [in Chinese]. Zhonghua Yi Yuan Gan Ran Xue Za Zhi 22: 1150–1152.
- 98. Xie D, Xu X, Wang S (2007) The analysis of bacteria with extended spectrum beta-lactamases in incisional infections [in Chinese]. Xian Dai Zhong Xi Yi Jie He Za Zhi 16: 5121–5122.
- 99. Xie M, Yan W, Xiong J (2008) Pathogen distribution and drug resistance in postoperative incisional infections [in Chinese]. Zhonghua Yi Yuan Gan Ran Xue Za Zhi 18: 874–876.
- 100. Xie DS, Xiong W, Xiang LL, Fu XY, Yu YH, et al. (2010) Point prevalence surveys of healthcare-associated infection in 13 hospitals in Hubei Province, China, 2007–2008. J Hosp Infect 76: 150–155. pmid:20692727
- 101. Xie X, Yang C, Bi J, Chen W, Zhou J (2012) Pathogens causing surgical site infections and drug resistance [in Chinese]. Zhonghua Yi Yuan Gan Ran Xue Za Zhi 22: 4387–4389.
- 102. Xiu Y, He T, Wang Y, Yao Y (2012) Analysis on drug-resistance pathogens in Class Ⅰ surgical wound infections [in Chinese]. Hu Li Yan Jiu 26: 2631–2633.
- 103. Xu M, Shi Z, Tang M, Zhou J (2007) Distribution and antimicrobial resistance of bacteria isolated from cerebral spinal fluid in neurosurgical patients: a ten years surveillance [in Chinese]. Beijing Yi Xue 29: 583–586.
- 104. Xu X, Huang Z, Liu J (2010) Distribution and drug resistance of bacteria isolated from postoperative infections in orthopedic patients [in Chinese]. Zhonghua Yi Yuan Gan Ran Xue Za Zhi 20: 1304–1306.
- 105. Xu Y (2011) The causative analysis on incisional infections after abdominal operation in 31 cases [in Chinese]. Zhong Wai Jian Kang Wen Zhai 8: 181–182.
- 106. Yan B, Li M, Xu X (2008) The distribution and antimicrobial resistance of pathogenic oganism in surgical site Infections [in Chinese]. Jiangxi Yi Xue Yuan Xue Bao 48: 49–51, 55.
- 107. Yang C (2009) Surgical incisional infections in a rural hospital in the impoverished area [in Chinese]. Zhonghua Yi Yuan Gan Ran Xue Za Zhi 19: 1512–1513.
- 108. Yang X, Zhang Y, Guo T, Li X (2009) Monitoring survey about the incisional infections after surgery in 46 cases [in Chinese]. Xian Dai Yi Yao Wei Sheng 25: 1676–1678.
- 109. Yao D (2011) Distribution of pathogens from infected surgical incisions in colorectal cancer and its influencing factors [in Chinese]. Zhongguo Xian Dai Yi Sheng 49: 147–148, 154.
- 110. You H, Liao C, Yang X, Shan Z, Zhao X, et al. (2011) Risk factors of surgical site infections in adult patients after cardiopulmonary by-pass surgery [in Chinese]. Zhonghua Yi Yuan Gan Ran Xue Za Zhi 21: 894–896.
- 111. Yu Y, Chen Z (2012) Hospital surgical site infections: distribution of pathogens and detection of drug resistance [in Chinese]. Zhonghua Yi Yuan Gan Ran Xue Za Zhi 22: 1282–1284.
- 112. Yue X (2009) The clinical analysis on incisional infections after gynecologic surgery [in Chinese]. Zhongguo Shi Yong Yi Yao 4: 183.
- 113. Zeng L, Zhang C (2012) Drug resistance in pathogens causing surgical incisional infections after cesarean section and prevention measures [in Chinese]. Zhonghua Yi Yuan Gan Ran Xue Za Zhi 22: 1285–1286.
- 114. Zhang R, Yang Y (2007) Etiology and drug sensitivity analysis of wound infections in the department of orthopaedics [in Chinese]. Guo Ji Jian Yan Yi Xue Za Zhi 28: 25–27.
- 115.
Zhang Z, Cao Y (2008) Study on the isolation and drug resistance of common pathogenic bacteria in general surgery infections [in Chinese]. The Fifth Academic Conference of Analytic Microbiology Professional Committee of Hubei Microbiology Association. pp. 220–225.
- 116. Zhang X (2009) An analysis of the antimicrobial-resistant pathogens in surgical incisional intections [in Chinese]. Zhonghua Shi Yong Zhong Xi Yi Za Zhi 22: 1491–1492, 1494.
- 117. Zhang Y, Lv W (2009) Hospital postoperative infections: distribution of pathogens and detection of drug resistance [in Chinese]. Zhongguo Wei Sheng Jian Yan Za Zhi 19: 1315–1317.
- 118. Zhang X, Luo L (2010) Investigation and prevention of the risk factors of incision infection after abdominal operation [in Chinese]. Nanhua Da Xue Xue Bao 38: 301–302.
- 119. Zhang X, Peng F (2011) An investigation of the pathogens distribution and their drug resistance in 160 cases with incisional infections after a general surgery [in Chinese]. Yi Yao Qian Yan 1: 47.
- 120. Zhang Y, Qian X (2011) Incisional infections after abdominal operations: investigation and analysis [in Chinese]. Zhonghua Yi Yuan Gan Ran Xue Za Zhi 21: 695–696.
- 121. Zhang Y (2011) The related factors and the prevention of incisional infections in primary level hospital [in Chinese]. Xian Dai Yu Fang Yi Xue 38: 590–591.
- 122. Zhang J, Zhang J (2012) The distribution and drug resistance of the pathogens in incisional infections [in Chinese]. Zhongguo Lin Chuang Yan Jiu 25: 338–339.
- 123. Zhao W (2011) Investigation and analysis of incisional infection in general surgery department [in Chinese]. Zhonghua Yi Yuan Gan Ran Xue Za Zhi 21: 3849–3850.
- 124. Zhao X, Liang Y, Wang W, Zhang J (2011) Drug-resistance of pathogens isolated from operative incisions [in Chinese]. Zhongguo Shi Yong Yi Kan 38: 27–28.
- 125. Zheng S (2007) Characteristics and prevention of the incisional infections in urologic surgical procedures [in Chinese]. Xian Dai Yu Fang Yi Xue 34: 3799–3800.
- 126. Zheng H, Xie M (2011) Antimicrobial resistance of pathogens causing surgical site infections in suizhou and interventions [in Chinese]. Zhonghua Yi Yuan Gan Ran Xue Za Zhi 21: 601–602.
- 127. Zheng H (2011) Risk factors for abdominal surgical wound infections and pathogenic bacteria investigation [in Chinese]. Zhonghua Yi Yuan Gan Ran Xue Za Zhi 21: 270–271.
- 128. Zheng S, Peng G, Xie L, Zhang C (2011) Pathogens causing wound infections after pediatric surgery and drug resistance [in Chinese]. Zhonghua Yi Yuan Gan Ran Xue Za Zhi 21: 5310–5312.
- 129. Zhou B, Li C (2007) Distribution and drug resistance of pathogenic bacteria in incisional wounds in puerperae [in Chinese]. Zhongguo Re Dai Yi Xue 7: 2144–2146.
- 130. Zhou B, Li C (2008) Clinical analysis of 18 cases with abdominal incisional infectons after cesarean section [in Chinese]. Shi Yong Fu Chan Ke Za Zhi 24: 436–437.
- 131. Zhou J, Wen X (2011) Distribution and drug resistance of the pathogens in incisional infections after surgery in Shiyan area [in Chinese]. Jian Yan Yi Xue Yu Lin Chuang 8: 972–974.
- 132. Zhou Y, Tian P, Du W, Rong Y (2011) Effect of linezolid for the Gram-positive cocci infections in sternum osteomyelitis [in Chinese]. Zhonghua Sun Shang Yu Xiu Fu Za Zhi 6: 50–51.
- 133. Zhu J, Tong H (2007) Investigation of surgical site infections after abdominal surgery in our hospital in recent 5 years [in Chinese]. Ji Ceng Yi Xue Lun Tan 11: 485–486.
- 134. Zhu Y, Wang L (2008) Distribution and drug resistance of pathogenic bacteria in surgical wounds of orthopedic surgery [in Chinese]. Zhongguo Xian Dai Yi Yao Za Zhi 10: 121–122.
- 135. Zhu Z, Zhu P, Shao J, Li H, Mao S (2008) Detection of pathogens and antimicrobial resistance in surgical incisional infections [in Chinese]. Zhonghua Yi Yuan Gan Ran Xue Za Zhi 18: 1186–1188.
- 136. Zhu H, Ke Y, Lin X, Zhou N (2010) Infection outbreak caused by mycobacterim abscess after cesarean section [in Chinese]. Zhongguo Gan Ran Kong Zhi Za Zhi 9: 393–395.