Global prevalence and antibiotic resistance in clinical isolates of Stenotrophomonas maltophilia: a systematic review and meta-analysis

Abstract

Introduction:

Stenotrophomonas maltophilia is a little-known environmental opportunistic bacterium that can cause broad-spectrum infections. Despite the importance of this bacterium as an emerging drug-resistant opportunistic pathogen, a comprehensive analysis of its prevalence and resistance to antibiotics has not yet been conducted.

Methods:

A systematic search was performed using four electronic databases (MEDLINE via PubMed, Embase, Scopus, and Web of Science) up to October 2019. Out of 6,770 records, 179 were documented in the current meta-analysis according to our inclusion and exclusion criteria, and 95 studies were enrolled in the meta-analysis.

Results:

Present analysis revealed that the global pooled prevalence of S. maltophilia was 5.3 % [95% CI, 4.1–6.7%], with a higher prevalence in the Western Pacific Region [10.5%; 95% CI, 5.7–18.6%] and a lower prevalence in the American regions [4.3%; 95% CI, 3.2–5.7%]. Based on our meta-analysis, the highest antibiotic resistance rate was against cefuroxime [99.1%; 95% CI, 97.3–99.7%], while the lowest resistance was correlated with minocycline [4·8%; 95% CI, 2.6–8.8%].

Discussion:

The results of this study indicated that the prevalence of S. maltophilia infections has been increasing over time. A comparison of the antibiotic resistance of S. maltophilia before and after 2010 suggested there was an increasing trend in the resistance to some antibiotics, such as tigecycline and ticarcillin-clavulanic acid. However, trimethoprim-sulfamethoxazole is still considered an effective antibiotic for treating S. maltophilia infections.

Introduction

Stenotrophomonas maltophilia is an environmental Gram-negative bacillus that has been the subject of extensive research over the last two decades due to its status as the only known species of Stenotrophomonas to cause opportunistic infections in humans (1). Before the 1970s, this bacterium was underestimated and was considered a rare opportunistic pathogen with low invasiveness. However, advances in medical interventions and pharmacological treatments have led to an increase in the population of immunocompromised patients, such as those undergoing chemotherapy, organ transplantations, or complex surgeries, who are prone to infection with this bacterium. In addition, the development of diagnostic methods in clinical microbiology resulted in more precise identification of this pathogen. Therefore, the number of reported S. maltophilia infections has increased, and it is recognized as an emerging nosocomial pathogen (2). S. maltophilia causes infections of the soft tissue, urinary tract, eye, and wound. In addition, it causes pneumonia, bacteremia, sepsis, endocarditis, osteochondritis, mastoiditis, and meningitis (3). Predisposing factors associated with S. maltophilia infections include underlying malignancy, indwelling devices, chronic respiratory disease, particularly cystic fibrosis, immune compromisation, prolonged antibiotic use, and long-term hospitalization or admission to an intensive care unit (ICU) (3, 4). The treatment of infections caused by this bacterium presents several challenges. Distinguishing colonization from invasive infections is problematic, and physicians often fail to recognize their associated risk factors and clinical characteristics, which leads to delayed antibiotic prescription and high mortality (5).

Because of the high-level intrinsic resistance of S. maltophilia to several classes of antibiotics, there are restricted therapeutic choices for its infections. This bacterium can resist the β-lactam antibiotics (most notably carbapenems) by producing ß-lactamase enzymes, including L1 and L2. It also disrupts the action of aminoglycosides by hydrolyzing enzymes such as acetyl-transferases or modifying the structure of lipopolysaccharide. In addition, low membrane permeability and the overproduction of efflux pumps are other mechanisms that render S. maltophilia resistant to a broad range of antibiotics (2, 6). Additionally, they can acquire resistance genes and genetic mutations (7, 8), further limiting the choice of effective antimicrobials. This increasing prevalence of drug-resistant S. maltophilia has presented one of the biggest challenges in treating patients in recent years (3, 9).

The Infectious Diseases Society of America (IDSA) has approved a guideline document with recommendations for treating S. maltophilia infections (10). Trimethoprim-sulfamethoxazole (TMP/SMX) is the antibiotic of choice for treating these infections, but its use is limited by allergy, intolerance, and increased resistance (11). Other drugs with good susceptibility impact include ticarcillin-clavulanate, ceftazidime, and fluoroquinolones, although resistance to these drugs has been reported. Tetracyclines such as minocycline, tigecycline, and doxycycline are also efficacious in treating S. maltophilia infections, and their efficacy has been reported in different geographic areas (3, 12).

The main objective of this study was to assess the global prevalence of S. maltophilia and its resistance to commonly used antibiotics. We conducted this systematic review of global human infections due to S. maltophilia over the last 31 years.

Methods

Search strategy and selection criteria

Four electronic databases, including MEDLINE (via PubMed), Embase, Web of Science, and Scopus, were systematically searched using different combinations of the following keywords: “Stenotrophomonas maltophilia” OR “Xanthomonas maltophilia” AND “antibiotic resistance” AND “minimum inhibitory concentration” AND “disk agar diffusion” AND “multilocus sequence typing” AND “E-test” AND “antimicrobial resistance gene”. The databases were searched up to 20 October 2019 without any start time limitation.

The study was carried out based on the guidelines of the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) (13). Two distinct reviewers applied the inclusion and exclusion criteria for article selection and screened the titles and abstracts of all studies; then, two autonomous researchers qualified the screened papers. Any disagreements between the reviewers were resolved by consensus.

Inclusion criteria

Articles were included if they reported the prevalence of S. maltophilia isolation among diverse patients in combination with the antibiotic resistance rates of the isolates to various antibiotics, or reported only the antibiotic resistance rates of the isolates. Only articles about the clinical isolates of S. maltophilia were enrolled, and studies on the environmental isolates were not considered.

Exclusion criteria

Conference papers were not evaluated as they did not provide sufficient information for quality assessment. Dissertations and theses were excluded. Articles with unrelated topics, duplicates or overlapping studies, reviews, meta-analyses or systematic reviews, case reports, brief reports, notes, editorials, correspondence, short communications, and letters to the editors were not included. Studies with languages other than English or with unavailable full text were dismissed. Studies that evaluated species other than S. maltophilia or tested a total isolate <10 were not assessed. Articles that reported antibiotic resistance as MIC 90 or those that evaluated the combinatorial effects of antibiotics were not enrolled. Studies that considered S. maltophilia a Gram-negative bacterium and reported a total antibiotic resistance rate in Gram-negative bacteria were excluded. Articles were removed if they tested only the resistant isolates or reported only the prevalence of S. maltophilia infection.

Study selection and data extraction

Two independent researchers read the included articles in full text and extracted the following details: first author's name, year of study, year of publication, location of the study (country and region), sample size (N/total), type of samples, antibiotic susceptibility testing methods used (agar dilution, broth microdilution, broth macrodilution, E-test, disk agar diffusion [DAD], MIC test strip, Vitek, Phoenix, and Microscan), the antibiotic resistance rate of isolates against various antibiotics, frequency of resistance genes, and frequency of different sequence types. Any discrepancy between the two reviewers was settled by consensus.

Quality assessment

Two reviewers separately evaluated the quality of the included studies using the Joanna Briggs Institute (JBI) critical appraisal checklist for studies reporting prevalence data (14). This scale rates each criterion out of 1, with a total score ranging from 0 to 10. Studies with a score of ≥5 were classified as high quality.

Meta-analysis

The meta-analysis was carried out using Comprehensive Meta-Analysis (CMA) software version 2.0 (Biostat, Englewood, NJ). A random-effect model was used for meta-analysis and to pool the estimations. The prevalence of the investigated phenomenon was presented as a forest plot diagram, which shows the estimated prevalence and its relevant 95% confidence interval (CI). Heterogeneity between studies was reported by I² statistics. An I² between 0 and 25% suggests low heterogeneity, 25–50% indicates moderate heterogeneity, 50–75% represents substantial heterogeneity, and 75–100% shows considerable heterogeneity. Subgroup meta-analysis was employed to compare the prevalence of S. maltophilia based on WHO-defined regions and 5-year time intervals. In addition, the antibiotic resistance rates of isolates were compared based on world regions and whether they were reported before or after 2010. To assess the potential risk of publication bias, Begg's rank correlation and Egger's weighted regression methods in combination with a funnel plot were used (P < 0.05 was regarded as indicative of a statistically notable publication bias) (15).

Results

A total of 6,770 records were identified through searches of the four aforementioned electronic databases (Figure 1). After removing the 3,613 duplicates, 3,157 unique records were screened based on titles and abstracts, and 2,340 articles were excluded, such as studies with non-relevant topics (n = 1,245), repetitive articles (n = 470), reviews (n = 234), systematic reviews (n = 3), case reports (n = 64), letters to the editors (n = 60), conference abstracts (n = 111), editorials (n = 9), short surveys (n = 10), correspondence (n = 2), notes (n = 12), reports (n = 3), a book (n = 1), articles with a total sample of <10 strains (n = 17), non-English studies (n = 47), and articles that studied environmental samples (n = 21). In addition, 30 articles were removed because their full texts were not available. The eligibility of 817 full-text articles was assessed and, ultimately, 179 studies met the inclusion criteria and were enrolled in the qualitative analysis. Of these, 95 studies reporting the prevalence of S. maltophilia infection were selected for quantitative analysis (meta-analysis). The characteristics of the 179 included studies are summarized in Table 1.

Figure 1

Overall, 179 studies conducted during the 31-year period between 1986 and 2017 were included. The articles had a wide geographical distribution, and the studies featured in them were carried out in different parts of the world. According to the World Health Organization's (WHO) regions, most studies were from the European Region (n = 57, 32%), followed by the West-Pacific Region (n = 39, 22%), the Region of the Americas (n = 37, 21%), the Eastern Mediterranean Region (n = 14, 8%), and the South-East Asian Region (n = 8, 4%). There was no independent study from the African Region. Twenty-four studies (13%) were conducted across different continents and were, therefore, classified as multiple region studies and did not conform to the WHO categories (Table 1).

The studies had very different sample sizes, ranging from 10 to 130,033. A total of 580,963 samples were examined, of which 25,596 were positive for S. maltophilia. Of the 179 studies, only 58 reported the types and details of examined specimens (5,106 samples). The most frequent sources of S. maltophilia isolation were respiratory samples (n = 3,434, 67%) and blood (n = 1,223, 24%) (Table 1). The qualities of all the reviewed studies were evaluated using the JBI critical appraisal checklist. Of the 95 studies included in the meta-analysis, 78 (82%) scored seven, 16 (17%) scored six, and one (1%) scored five. Therefore, all the studies enrolled in the meta-analysis had a high-quality score (a score of five or more) (Table 1).

Prevalence of Stenotrophomonas maltophilia by WHO regional offices

Based on the meta-analysis, the pooled prevalence rate of global S. maltophilia infection was estimated to be 5.3 % [95% CI, 4.1–6.7%] (Table 2 and Figure 2). Egger's test did not demonstrate publication bias (P > 0.05). However, Begg's test showed evidence of publication bias in the 95 analyzed studies (P = 0.017). Additionally, the corresponding funnel plot indicated publication bias (Supplementary File 1). Results demonstrated high heterogeneity (I²= 99.428%; P = 0.000) among the selected studies (Table 2).

Figure 2

Subgroup meta-analysis based on the publication period of the studies (from 1991 to 2019) revealed that the prevalence rate of S. maltophilia isolation had an increasing trend over time, from 1.7% [95% CI, 0.7–4%] between 1991 and 1995 to 6.5% [95% CI, 4.1–10.1%] between 2016 and 2019. The highest prevalence rate [7.7%; 95% CI, 4.3–13.4 %] was observed between 2011 and 2015 (See Figure 3 and Table 3) (Supplementary File 1).

Figure 3

Subgroup meta-analysis based on the world regions defined by WHO revealed that the highest prevalence of S. maltophilia infections occurred in the Western Pacific Region [10.5%; 95% CI, 5.7–18.6%] and the European Region [7.9%; 95% CI, 4.3–14%]. The lowest prevalence occurred in the Region of the Americas [4.3%; 95% CI, 3.2–5.7%] (see Table 3 and Figure 4).

Figure 4

Evaluation of the regional prevalence of S. maltophilia isolation based on the publication time of studies (from 1991 to 2019) showed an overall increasing trend. In the Western Pacific Region, the prevalence rate of S. maltophilia decreased from 2006 to 2010; however, the prevalence rates in the European Region and the Regions of America increased after this time interval (Figure 5 and Supplementary File 1).

Figure 5

The antibiotic resistance rate of Stenotrophomonas maltophilia

The susceptibility of S. maltophilia isolates to various antibiotics was determined using various methods, including broth micro-dilution, broth macro-dilution, agar dilution, disk agar diffusion (DAD), E-test, and automated methods (e.g., VITEK, Phoenix, and micro-scan systems). Broth micro-dilution was the most frequently used assay. The standards used for interpreting the results of susceptibility assays varied, with different breakpoints used, such as those of the Clinical and Laboratory Standards Institute (CLSI), National Committee for Clinical Laboratory Standards (NCCLS), European Committee on Antimicrobial Susceptibility Testing (EUCAST), U.S. Food and Drug Administration (FDA), British Society for Antimicrobial Chemotherapy (BSAC), TRUST, and Comité de l'Antibiogramme de la Société Française de Microbiologie (CA-SFM) (Supplementary File 2).

As shown in Table 4, the highest resistance rates of S. maltophilia isolates were to cefuroxime [99.1%; 95% CI, 97.3–99.7%], cefoxitin [96.5%; 95% CI, 80.9–99.4%], ampicillin [96.1%; 95% CI, 92.8–97.9%], imipenem [94.9%; 95% CI, 92.3–96.7%], and meropenem [93.3%; 95% CI, 87.2–96.6%], while the lowest resistance rates were to doxycycline [5.7%; 95% CI, 3.3–9.7%] and minocycline [4.8%; 95% CI, 2.6–8.8%].

A comparison of antibiotic resistance rates of S. maltophilia before and after 2010 (Figure 6) revealed an increasing trend for some antibiotics, such as chloramphenicol (12.3%), TMP/SMX (11.6%), ceftazidime (8.6%), and levofloxacin (1.8%). Conversely, the resistance rate against minocycline (2.2%) decreased.

Figure 6

The results of the subgroup meta-analysis based on the world regions and antibiotic resistance rates, presented in Figures 7–9, as well as in Supplementary File 1, showed that the highest resistance rate across all regions was to ceftazidime, while the lowest rate was to minocycline.

Figure 7

Figure 8

Figure 9

Discussion

Although S. maltophilia shows limited invasiveness in immunocompetent individuals, it can lead to severe infections in immunocompromised patients. Moreover, its high intrinsic resistance to a large number of antimicrobial agents results in treatment failure and mortality in patients infected by this microorganism (191–194). Thus, the undertaking of a first systematic review and meta-analysis addressing the prevalence rate of isolation and antibiotic resistance rates of S. maltophilia in different regions of the world may be of great value in managing infections caused by this bacterium.

Based on the present meta-analysis, most studies were reported from the European Region (n = 57, 32%), while in a similar investigation (12), the majority of cases were reported and managed in the United States of America (n = 72, 27.7%). The differences between the inclusion and exclusion criteria applied in these two studies may explain the differing results. In the current study, the global prevalence rate of S. maltophilia isolation from clinical samples was 5.3%, and according to the WHO classification, the highest prevalence rate of S. maltophilia isolation was observed in the Western Pacific Region (10.5%), followed by the European Region (7.9%), which may be due to their long-shared land border. Among the reasons for the discrepancies in the prevalence of Stenotrophomonas maltophilia infection in different world regions, we can mention the following: disparate health policies in each country affect the importance of pathogens, so, in some countries, Stenotrophomonas maltophilia is still considered an unimportant opportunistic pathogen, so few studies have been reported. For example, most of the cases were documented in European (195), Asian (86), and American (196) countries, while there was no relevant study performed in the African continent. This difference can cause publication bias and affect the overall results. Additionally, the differences in health levels of various countries and the numbers and types of examined patients all influence the reported prevalence of Stenotrophomonas maltophilia.

In this meta-analysis, among different clinical samples, respiratory samples were the most frequent source (67%), followed by blood samples (24%). This finding is consistent with other studies, in which S. maltophilia was most commonly associated with respiratory tract infections, followed by bloodstream infections (74, 197). However, in another systematic review, blood was the most prevalent site of S. maltophilia isolation (12). In a large study performed in the USA and fifteen centers in European countries in 2012, 6.3% of the isolates obtained from respiratory tract infections were identified as S. maltophilia. These data suggest that the rate of respiratory tract infections caused by S. maltophilia is increasing (3, 198). The bacterium's capability for adherence to plastic surfaces and biofilm formation on hospital devices, such as those inserted into the respiratory tract, may explain its high rate in the aforementioned samples (199, 200). For example, among patients with ventilator-associated pneumonia (VAP), the most common nosocomial infection in mechanically ventilated patients, S. maltophilia is the probable causative pathogen (196, 201). Moreover, its adaptation to the airways of individuals with cystic fibrosis (CF) has led it to being recognized as an emerging multi-drug resistant opportunistic pathogen (86).

The prevalence rate of infections caused by this bacterium increased from 1.7% to 6.5% during the 31 investigated years, suggesting that it is emerging as an opportunistic pathogen, particularly among immunocompromised hosts. This rapid rise may be due to its resistance to a wide range of antimicrobial agents, as well as the increased focus on this bacterium as a cause of infection. The treatment of S. maltophilia infections is challenging due to the difficulty of differentiating colonization from infection and the intrinsic resistance of this bacterium to multiple classes of antibiotics. The WHO has classified S. maltophilia as one of the leading multidrug-resistant organisms in hospital settings (202). Additionally, recent antibiotic treatment and other known factors associated with acquiring S. maltophilia infections demonstrate specific features of this bacterium (195).

Based on our data, the highest and the lowest global resistant rates were to cefuroxime and minocycline, respectively (Figure 3). The lowest resistance to TMP-SMX was observed in the EMR (4.5%) and AMR (13.1%), while in other geographical regions, resistance was higher than 20%. Consequently, TMP-SMX may be the first choice for treatment based on antibiotic susceptibility and therapeutic success (3, 60, 203). Fortunately, in the present study, a comparison of global antibiotic resistance rates of S. maltophilia before and after 2010 (Figure 4) confirmed the effectiveness of this medication for treating infections of this opportunistic organism. However, there is not always a logical correlation between laboratory sensitivity and clinical results. Other antibiotics for treating Stenotrophomonas infections include fluoroquinolones, tetracyclines, and selected β-lactams, such as ceftazidime and ticarcillin/clavulanate. However, the development of resistance to some of these antibiotics renders them unreliable.

Fluoroquinolones are prescribed for treating infections caused by TMP-SMX-resistant S. maltophilia and for patients for whom this drug has adverse effects. Studies comparing treatments with fluoroquinolones and TMP-SMX have proposed that levofloxacin has similar effectiveness with fewer adverse effects than TMP-SMX (204, 205). Our study indicates that resistance rates to levofloxacin vary geographically, ranging from 6.4% in EMR to 15%−22% in EUR, AMR, and WPR, and up to 26% in SEAR. However, the rapid emergence of resistance against quinolones in vitro and in vivo is of concern when levofloxacin is used to treat S. maltophilia infections.

In surveillance studies of the efficacy of tigecycline and related tetracycline antibiotics, minocycline was found to be effective against S. maltophilia (206). In this study, resistance to minocycline was <10% in all geographical areas and global resistance to tigecycline was 11.8%. A comparison of the antibiotic resistance rates of S. maltophilia before and after 2010 revealed an increase in resistance to tigecycline from 4.1% to 18.6%. Several studies have revealed that minocycline is not inferior to TMP-SMX and may even be more suitable than TMP-SMX in terms of susceptibility. These results suggest that minocycline and TMP-SMX may be the first-line therapy in S. maltophilia infections, even in TMP-SMX-resistant strains (59).

Ceftazidime and ticarcillin/clavulanate have previously been reported as the most effective β-lactam drugs against S. maltophilia. However, reduced sensitivity to ceftazidime has been documented in recent studies. Owing to β-lactamase production, a high resistance rate to β-lactams such as cefuroxime, cefoxitin, imipenem, and meropenem (> 90%, Table 4) has been observed, thus reducing their role in the treatment of S. maltophilia infections (207). According to this analysis, ceftazidime has a high resistance rate in all regions classified by the WHO (AMR, 56.4%; EMR, 42.9%; SEAR, 65.1%; WPR, 52.6%). Our study suggests that the rate of resistance to ticarcillin/clavulanate globally is 33.2%. Therefore, these current resistance rates to ceftazidime and ticarcillin/clavulanate render them unreliable. However, the use of ceftazidime in combination with other antibiotics (typically vancomycin, amikacin, TMP-SMX, or fluoroquinolones) is an effective treatment for infections caused by S. maltophilia (13). A systemic literature review by Gibb and Wong (208) offers recommendations for a treatment strategy for Stenotrophomonas infection based on current evidence. The first-line drugs suggested are TMP-SMX, fluoroquinolones, and tetracyclines.

Our study presents several limitations. First, a large number of the included studies (84 articles) evaluated a specific number of S. maltophilia isolates but did not report the prevalence rate of isolation; thus, these studies were not included in the meta-analysis, which could affect the pooled prevalence rate of S. maltophilia isolation and the antibiotic resistance rates. Second, the number of published studies reporting the resistance mechanism of strains isolated from clinical samples (see Supplementary File 2) is relatively small, and the specific genes conferring antibiotic resistance in these isolates remain unclear. Third, a few studies used typing methods to evaluate S. maltophilia isolates (see Supplementary File 2), so we could not report the most prevalent types of this bacterium at the global and regional levels.

Conclusion

In conclusion, despite the undeniable clinical impact of S. maltophilia, compared with other Gram-negative species, this bacterium is remarkably understudied. Thus, collecting and analyzing data related to different aspects of S. maltophilia may assist in improving the clinical management of challenges caused by this bacterium. This meta-analysis presents the global antibiotic resistance of S. maltophilia over the last 31 years and demonstrates different rates of resistance in world geographical regions, as well as the growing trend of resistance to most antibiotics. The variations in antibiotic resistance of S. maltophilia isolates in different regions may be the result of the use of different protocols for patient treatment. Additionally, the improper and experimental use of antibiotics plays an important role in increasing resistance, leading to an increased risk of treatment failure. To address this issue, it is necessary to carry out antibiotic sensitivity tests before prescribing antibiotics and implementing an antimicrobial stewardship program for every hospital, as well as provide continuous training for clinicians about their performance in the hospital environment. Finally, collecting and preparing local sensitivity patterns will be effective in allowing the selection of the optimal empiric treatment for S. maltophilia infections.

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