Identification and characterization of SCCmec typing with psm-mec positivity in staphylococci from patients with coagulase-negative staphylococci peritoneal dialysis-related peritonitis
BMC Microbiology volume 23, Article number: 267 (2023)
Peritonitis is the most important complication of peritoneal dialysis (PD) and coagulase-negative staphylococci (CNS) are a frequent cause of dialysis-related infections. The association between SCCmec typing with psm-mec positivity in staphylococci and PD-related infections has not been identified. We aim to investigate the molecular epidemiology of CNS isolated from PD-peritonitis in a single Chinese center, focusing on the genetic determinants conferring methicillin resistance.
We collected 10 genetically unrelated CNS isolates from 10 patients with CNS PD-related peritonitis. The patients were divided into two groups based on the results of MIC to oxacillin: the methicillin-resistant CNS (MRCNS) and methicillin-sensitive CNS (MSCNS) groups. The biofilm formation group (BFG) and the non-biofilm formation group (NBFG) were used as the control groups. Phenotypic and molecular methods were used to analyze SCCmec types I, II and III, associated genes and biofilm formation and the existence of psm-mec. The demographic data and clinical indicators were collected.
Ten CNS PD-related peritonitis patients were enrolled for this study. There were 6 MRCNS and 4 MRCNS isolates. SCCmec types were fully determined in 10 isolates. Seven staphylococci (70%) carried SCCmec, of which 4 isolates carried single SCCmec type I (40%) and 3 isolates had multiple SCCmec elements (I + III). Of the 6 MRCNS isolates, 3 carried SCCmec type I (50%) and 2 isolates carried SCCmec type I + III (33.3%). A high diversity of ccr types, mec complexes and ccr-mec complex combinations was identified among the 10 CNS isolates. The psm-mec gene was detected in 2/10 (20%) CNS isolates. There was no mutation in the psm-mec gene.
The majority of isolates were hospital-associated isolates. Furthermore, 2 psm-mec positive isolates were MRCNS in the NBFG. The PD patients frequent exposure to hospital would be the main risk factor. The presence of the psm-mec signal in the spectra of the MRCNS tested here demonstrates the presence of certain SCCmec cassettes that convey methicillin resistance.
Peritonitis is one of the most important complications of peritoneal dialysis (PD). It is still the main reason for patients to transfer from PD to hemodialysis . Over the last few decades, the incidence of peritonitis caused by gram-positive pathogens in PD has decreased significantly, predominantly due to improvements in PD connectology system . However, gram-positive peritonitis, particularly Staphylococcus epidermidis and other coagulase-negative staphylococci (CNS), remains a common cause of dialysis-related infections . Staphylococci (S) warneri, S. hominis, S.haemolyticus, S.saprophyticus, S.capitis and S.simulans are staphylococcal species that have also been reported as infectious agents associated with PD . Contamination at the time of PD fluid exchange is thought to be a major cause of peritonitis, mainly from external sources . Many patients with CNS peritonitis have mild clinical symptoms. They respond well to outpatients treatment . Relapsing CNS peritonitis suggests that the PD catheter has biofilm formation, and removal of the catheter should be considered . The characteristics of CNS infections are increasing rates of antibiotic resistance. Colak documented that approximately 70% of methicillin-resistant coagulase-negative staphylococci (MRCNS) are involved in CNS peritonitis . A previous study also identified methicillin resistance as an independent predictor of failure in CNS caused PD-related peritonitis .
In Staphylococci, the presence of PBP2a, encoded by the mecA gene, is responsible for resistance to β-lactam antibiotics . This gene, known as the staphylococcal cassette chromosome mec (SCCmec), is related to a mobile genetic element (MGE) . The unique combination of the mec gene complex class and the cassette chromosome recombinase (ccr) gene complex type determines the type of the SCCmec, and its variation within the junctional- (J-) regions determines the subtypes of each SCCmec type . Currently, two unique ccr gene complexes have been described based on the assemble of ccr genes. One carries two adjacently located ccr genes, ccrA and ccrB, and the other carries ccrC. The ccrA and ccrB genes in S. aureus strains have been classified into four and five subtypes respectively, which lead to six ccr gene complex types referred to as type 1 (ccrA1B1), type 2 (ccrA2B2), type 3 (ccrA3B3), type 4 (ccrA4B4), type 7 (ccrA1B6) and type 8 (ccrA1B3). In contrary, all ccrC variants were identified with a high nucleotide similarity and derived from two allotypes, ccrC1-2,which constitute types 5 and 9 of the ccr gene complex . To date, 14 different types of SCCmec have been identified with a number of different types and variations . These cassettes are characterized by a high degree of diversity in the sequence and in the mobile elements that are integrated into them.
Phenol-soluble modulins (psm)-mec is a peptide that is excreted in small amounts. They are carried on three SCCmec cassettes (types II, III and VIII) which contain the class A mec gene complex . Psm is a small peptide toxin that is considered to be a key virulence determinant in promoting pro-inflammatory processes and human cell lysis . Moreover, some PSMs promote biofilm formation. Previous studies have also documented the existence of psm-mec gene in clinical isolates of methicillin-resistant S. epidermidis (MRSE) . In addition, most MRSE have strong biofilm formation ability. Therefore, we speculate that psm-mec may also control biofilm formation of CNS isolates from patients with CNS PD-associated peritonitis. However, no relevant reports have been available until now. The aim of this study, was to investigate the role of psm-mec in CNS isolates from patients with CNS PD-related peritonitis biofilm formation, we evaluated 10 genetically unrelated CNS isolates from patients undergoing CNS PD-related peritonitis in relation to SCCmec types I, II and III; associated genes; and biofilm formation and the existence of psm-mec to understand the type of SCCmec among staphylococci to discover from which species different elements.
Between July 2019 and September 2021, 10 PD patients were recruited at Haikou People’s Hospital. The inclusion criteria as previously described were as follows : (1) patients over 18 years old; (2) Continuous treatment with PD for more than 3 months and a stable clinical condition during the period of observation; (3) patients with CNS PD-related peritonitis during their time on PD; and 4) informed approval. PD patients with recent use of antimicrobials, previous hospitalization, tuberculosis, cirrhosis, severe hepatitis and tumor, were excluded.
The diagnosis of CNS-associated peritonitis was made as previously described on the basis of three of the following criteria : (1) the presence of abdominal pain or the cloudiness of PD effluent; (2) white blood cell count in dialysis fluid > 100/µL with > 50% polymorphonuclear cells;(3) PD effluent (PDE) CNS positive culture. At least one of the first two criteria was present, and the third item was only required condition.
For all patients, demographic data and clinical indicators were collected. These indicators were surveyed on admission.
The microbiological tests were performed by centrifuging 50 mL of PDE was centrifuged at 3000 × g for 15 min and the pellet was seeded into Bact/Alet aerobic and anaerobic flasks (BioMerieux, Durham, NC, USA).The bacteria isolation and culture were performed in according with “National Clinical Practice Guidelines”. CNS were detected by using the VITEK − 2 automatic bacterial identification system and MALDI Biotyper Microflex LT/SH instrument (Bruker Daltonik GmbH, Bremen, Germany). Thus, CNS were instantly frozen at − 80 °C for testing.
Antimicrobial susceptibility test AND screening MRCNS
Drug sensitivity testing was performed using the VITEK − 2 MIC fully automatic bacterial identification instrument. The latest American CLSI (Clinical & Laboratory Standards Institute) test method and criteria were used. All isolates with a minimum inhibitory concentration (MIC) to oxacillin at a dose of ≥ 0.5 µg/mL were taken as MRCNS and ≤ 0.25 µg/mL as methicillin-sensitive CNS (MSCNS). The quality control strain used was Staphylococcus aureus.
Identification of CNS with biofilm formation
There were 2 cases of relapsing CNS peritonitis in this study. According to the 2016 ISPD recommendations, these cases should be considered CNS with biofilm formation . Two strains of relapsing CNS peritonitis have been verified as the same source by MLST.
DNA extraction from
The template was prepared by selecting 5 colonies to be assayed, which were resuspended in 500 µL of buffer heavy suspension cells and 50 µL of lysozyme. This suspension was heated in a water bath at 37 °C for 60 min and then centrifuged at 10,000 rpm for 1 min.
Determination of the mecA gene and SCC mec typing
The mecA gene was detected in all isolates using the polymerase chain reaction (PCR) method with the PCR primers showed in Table 1. The amplification was carried out in a volume of 25 µL of a total reaction mixture comprising 30 ng of template DNA, 12.5 µL of PCR supernatant and 1 µL of the following primer. The PCR conditions for amplifying prokaryotic 16 S fragments were an initial denaturation at 95 °C for 3 min; 35 cycles of a denaturation at 95 °C for 30 s, an annealing at 55 °C for 30 s and an extension at 72 °C for 1 min; and a completion extension at 72 °C for 5 min. 2% agarose gel electrophoresis was used to verify PCR products. To eliminate the possibility of false-positive PCR results, ultrapure water was substituted for sample solution as a negative control throughout the DNA extraction process. SCCmec types were determined for all CNS isolates by evaluating the mec and ccr gene complex. The typability of the SCCmec cassettes has been defined in the following way: (1) Typeable (T) SCCmec cassettes were those where ccr, mec complex type and/or SCCmec were determined; (2) Non-Ascribed (NA) SCCmec types were defined as those with a novel combination of ccr, mec complex and/or SCCmec. and (3) Non-typeable (NT) were those not positive with the primer according to the schedule. Those within the NA and NT categories were defined as New SCCmec .
The mecA genes were recovered from the overlapping regions after partial sequencing using BioEdit software. The mecA sequence from NZ_CP013911.1 (S167) was used as a reference and aligned with CLUSTALW as implemented in MEGA 6 (www.megasoftware.net). To check for mutations, the aligned sequences and their encoded proteins were then further analyzed.
Detection of psm-mec
The PCR was conducted on a Thermocycler (Sensoquest GmbH, Göttingen, Germany). The PCR primers were showed in Table 1. Psm-mec-for and Psm-mec-rev were used to detect the psm-mec gene.
SPSS 23.0 software package was used for data analysis. The data were expressed as the mean ± SD and comparisons were made by t-test. The χ2 or Fischer’s exact test was performed for all comparisons. Differences of P < 0.05 were considered statistically significant.
Between July 2019 and September 2021, 10 CNS PD-related peritonitis patients were enrolled There were 6 males and 4 females in the group. The average age was 56.17 ± 7.88 years, and the PD vintage was 27.5 ± 14.91 months. The pathogens were S. caprae in 3 patients, S. epidermidis in 4 patients, S. haemolyticus in 2 patients and S.capitis in 1 patient. The group was divided into two groups on the basis of the results of the MIC to oxacillin: the MRCNS and MSCNS groups. The biofilm formation group (BFG) and control group were formed. The BFG included CNS PD-related peritonitis patients with biofilm formation, while the control group was non-biofilm formation group (NBFG). A total of 6 MRCNS isolates and 2 BFG isolates were detected and confirmed to species in this study. In addition, we also found that there were more isolates within the NBFG were more in the MRCNS group than in the MSCNS group, although there was no significant difference (p = 0.053) (Table 2). The clinical characteristics and demographic of the patients are presented in Table 3.
Antimicrobial susceptibility of CNS
All CNS isolates were checked for susceptibility against 9 antibiotics using the disc diffusion test.6 out of 10 (60%) and 9 out of 10 (90%) isolates were resistant to oxacillin and penicillin respectively. Six isolates were resistant to erythromycin, whereas 4 (40%) isolates showed resistance towards erythromycin in the MRCNS group. Three (30%) isolates were resistant to azithromycin, and three (30%) were resistant to clarithromycin (Table 4). MRCNS isolates were resistant to azithromycin, followed by 2 (2/10; 20%) to clarithromycin, 1 (1/10; 10%) to cotrimoxazole, and 2 (2/10; 20%) to rifampicin and moxifloxacin (Table 4). Interestingly, in the BPCNS group the resistance rates towards oxacillin (0%) were comparatively low compared with BNCNS isolates, which exhibited a resistance towards oxacillin of 75% (p = 0.053) (Table 4).
Types of SCC mec types and multiple elements of SCC mec
The mecA gene was tested in 7/10 (70%) CNS isolates, 6/6 (100%) MRCNS isolates (Fig. 1a) and 7/8 (87.5%) NBFG isolates (Table 5). SCCmec types were fully determined in 10 isolates. Table 5 (Fig. 1a, b) shows the SCCmec typing results of these isolates. Those with two mecA classes were referred to as CNS with multiple SCCmec elements; CNSs with a single SCCmec element were considered to be those with one class of mecA complex and one class of ccr complex. Moreover, a new single SCCmec type was recovered only from 1 isolate (Table 6). Seven staphylococci (70%) carried SCCmec, followed by 4 isolates carrying a single SCCmec type I (40%) (Fig. 1b). Surprisingly, multiple SCCmec elements in 30% (3/10) of isolates. In particular, all isolates harboring five ccr complexes. Isolates had multiple SCCmec elements, especially all five ccr complexes. In all, 3 SCCmec cassettes were either NT or NA (30%) (Table 5). Of the 6 MRCNS isolates, 3 carried a single SCCmec type I (50%) and 2 isolates carried multiple SCCmec types (33.3%) (Table 5; Fig. 1c).
Unexpectedly, among these 4 CNS strains with no mecA segment detected, 2 strains contained a ccr complex (Table 6). In addition, 1 strain showed multiple ccr complexes. In this study, a grand total of 14 ccr complex segments were successfully aligned. No new ccr allotypes or new ccr alleles have been determined.5 isolates (50%) showed more than one type of ccr. The 2 ccrA1B1, 3 ccrA2B2, 2 ccrA3B3, 4 ccrA4B4 and 3 ccrC1 alleles from all CNS isolates were matched based on a BLAST search of GenBank sequences. Additional ccr genes (ccrA3B3, n = 1; ccrA2B2, n = 2) were also present in three SCCmec cassettes carrying ccrC1 (Table 5).
MecA sequencing and alignment
High homology with the mecA gene of the S. haemolyticus reference strain S167 was found in CLUSTALW (MEGA 6) among the 7 mecA genes sequenced from CNS isolates, However, no mutations were found (Table 5 and Supplemental material 1).
Detection of psm-mec
The psm-mec gene was detected in 2/10 (20%) CNS isolates. The pathogens were S. epidermidis and S.capitis. Moreover, they were all NBFG isolates. The phenotype of two isolates carrying psm-mec have been tested by ViteK2. We have observed their phenotypes were all MRCNS strains with multiple resistance. Furthermore, the phenotype is consisting with the genotype. Interestingly a combination of the class A mec complex and ccr type 3 was found in all these isolates. One of the two psm-mec positive isolates harboring SCCmec type I + III, accompanied by a combination of ccr types 3 and 5 and class A mec complex (Table 7). The psm-mec alleles were assigned on the basis of a BLAST search with sequences in GenBank, which revealed a homology of 99%, as shown in Supplemental material 2. There was no different the between two psm-mec alleles (Supplemental materials 3 and 4).
As far as we know, few studies have explored the correlation between the elemental compositions of SCCmec and the presence of psm-mec in CNS isolates from patients with CNS peritonitis. In the current study, the most common CNS in PD-related peritonitis was S.epidermidis, followed by S.caprae, S.haemolyticus and S.capitis. S. epidermidis are the most prevalent pathogens worldwide . In agreement with previous studies, we identified S. epidermidis as the predominant Staphylococcus species in patients with CNS PD-related peritonitis, accounting for 50% of cases. There were cases of 2 relapsing CNS peritonitis in this study. The pathogen in both cases was all S.capitis. A total of 6 MRCNS isolates and 2 BFG isolates were recovered. We also describe the antimicrobial resistance patterns and genetic variability of CNS in these patients. The resistance of CNS towards penicillin is well established. Rafatpanah et al.  revealed that 70% of recovered S. epidermidis isolates were resistance to penicillin. In accordance with their findings, we found that 90% of CNS isolates were genotypically resistant to penicillin. In the case of methicillin-resistant staphylococci, the mecA gene is involved in conferring resistance to almost all β-lactam molecules. Our study demonstrated that the resistance of CNS isolates to β-lactam antibiotics was higher. It is suggested that CNS peritonitis is characterized by a high rate of resistance to β-lactam antibiotic in our center. The mecA gene is determined methicillin-resistance in staphylococci, which is present in the SCCmec, leading to a reduced affinity for β-lactam antibiotics .
In general, the involvement of various types of SCCmec in the CNS depends on the geographical locations and host species . In our study, SCCmec typing allowed the differentiation between types I-III among the CNS strains. Our results showed a high rate of SCCmec I (40%), followed by SCCmec I + III (30%) (multiple SCCmec). Of the 6 MRCNS isolates, 3 isolates were carrier of SCCmec type I (50%), and 2 isolates were carrier of SCCmec type I + III (33.3%). SCCmec types I, II and III are most frequently associated with nosocomial infections resulting from methicillin-resistant staphylococci . However, SCCmec types IV and V are predominantly associated with community-acquired (CA) infections, SCCmec types I, II and III are markedly larger than the other types. It is suggested that the majority of isolates were hospital-associated (HA) CNS isolates in our study, especially for MRCNS. PD is basically a home treatment. Our findings therefore represent an interesting epidemiological situation, as the main risk factors associated with the development of drug-resistant bacteria (previous hospital admission, history of antimicrobials use) were not evident in our PD patients . We assumed that during frequent outpatient visit, routine consultations and some PD-related procedures of PD patients exposure to the hospital environment, may facilitate colonization by the hospital-associated CNS, leading to peritonitis and reaching the peritoneum within the dialysis procedure via intraluminal pathway or the periluminal (catheter-skin interface). Types I-III are relatively large in size and carry several antibiotic resistance determinants. Therefore, it can be interpreted that the CNS containing SCC elements in this study was also MRCNS. Types IV and V have been defined as new versions of SCCmec, which are short in length and generally do not carry any antibiotic resistance genes in association with the mec-gene complex . Unfortunately, we did not detect types IV and V SCCmec in this study.
In the last few years, more novel SCCmec elements, including non-mecA-encoding cassettes have been discovered in CNS. Surprising among these 4 CNS strains, one was now detected a mecA segment, but they were all MSCNS strains. Only 1 isolate carrying a new single SCCmec type was then examined in our study. There were 2 cases of relapsing CNS peritonitis in this study. However, they were all MSCNS strains. The absence of the SCCmec element was found in 1 isolate and 1 isolate with only ccr 4. The absence of the SCCmec element in CNS isolates may indicate extreme polymorphism . Samples containing only ccr or mec may be subject to recombination of the SCCmec element, insertion of a new structure, or structural re-arrangements . Furthermore, it is suggested that these 2 isolates are community-acquired (CA)-CNS strains based on the MSCNS isolates with new SCCmec. Szczuka et al. reported in S. aureus, S. epidermidis and other CNSs multiple copies of the ccr complex have been observed. However, the majority are a combinations of ccrAB and ccrC . Interestingly, the present study revealed different combinations of ccr types. 5 isolates (50%) showed more than one type of ccr. Furthermore, more than 1 ccr were also copresent in most of MRCNS, indicating that the clustering of the two ccr genes may confer an adaptive benefit. We observed three SCCmec cassettes with ccrC 1 that carried additional ccr genes (ccrA3B3, n = 1; ccrA2B2, n = 2). Few studies have explored a heterogeneous combination of ccr complexes in CNS strains, in particular all of the five types of ccr complexes that exist in the CNS strains from PD patients. Therefore, it was not unexpected that these CNS strains contained multiple SCCmec elements. The incidences of multiple SCCmec elements were as high as those observed in our study. For unveiling the actual presence and functionality of redundant ccr genes, and under specific conditions whether this indicates an adaptation advantage further analyses should be performed.
Psm-mec is not restricted to S. aureus, it has also been used to purify it from the culture suspension of MRSE. In particular, the gene psm-mec has been detected in other CNS . In present study the psm-mec gene was identified in 2/10 (20%) CNS isolates. The pathogens were S. epidermidis and S.capitis. Moreover, these isolates were all MRCNS. The results of this study revealed that the psm-mec gene was widespread within MRCNS strains. The existence of the psm-mec signal in the MRCNS spectra tested in our study indicates the existence of certain SCCmec cassettes which confer methicillin resistance. Consistent with previous studies, we found that 2 isolates with psm-mec positivity carried a combination of the class A mec complex and ccr types 3 and 5. More detailed studies showed that the psm-mec locus has been observed in SCCmec types II, IIA, IIB, IID, III, and VIII of a large number of Staphylococcus species . However, the types of SCCmec with psm-mec in present study were type I and I + III. This is the first study in which psm-mec was found in SCCmec type I, suggesting that SCCmec type I is a possible marker for analytical purposes. In agreement with previous studies the several widely distributed hospital-associated methicillin resistant S. aureus (HA-MRSA) lineages have been found to carry the psm-mec locus . CA-MRSA strains are genetically distinctive and significantly more invasive than HA-MRSA strains. Moreover, outside public healthcare institution these strains reveal elevated production of virulence factors, and are able to lead to disease from otherwise healthy individuals. Furthermore, CA-MRSA lacks the psm-mec locus. Our study suggested that these two isolates were HA-CNS strains based on their SCCmec types.
Interestingly, Qin et al. found CA-MRSA strains had a greater ability to disseminate on soft agar than HA-MRSA strains, and the deletion of the psm-mec locus in CA-MRSA strains was suggested to be responsible for this phenotype . Therefore, it will be possible to identify the origin of CNS harboring the psm-mec gene. PSM peptides have a significant effect on biofilm formation. PSMs lead to the structuring and biofilm maturation, which includes forming nutrient-transporting pathway . In contrast, 2 psm-mec positive isolates were NBFG isolates in the current study. A study investigating the absence of psm-mec in a mouse skin infection model either had not significantly change in virulence ,or decreased virulence. In addition, psm-mec has only a very small effects expressing other psm peptides. Since the region around psm-mec is well preserved in class A SCCmec elements, the author consider that the type of SCCmec element cannot influence the role of psm-mec in virulence . However, a recent study revealed that psm-mec may be involved as a virulence factor in S. epidermidis. This study was mainly on the basis of the study isogenous mutants of the psm-mec gene with clinical strains of S. epidermidis . Unfortunately, no psm-mec mutation was found in our study.
This study had several shortcomings. First, the size of the sample was rather limited; then, larger sample sizes are required in further studies. Second, we were unable to identify which ccr complex was associated with the particular SCCmec, especially when carrying multiple SCCmec. Third, the existence of multiple and untypable SCCmec elements poses a major challenge to SCCmec typing in CNS. Whole genome sequencing of more CNS would help construct new typing method by understanding the exact composition of multiple SCCmec and the relative location and further clarify the function of ccr complexes in the dissemination of SCCmec elements throughout CNS.
In summary, this study was the first study to determine the of frequency and diversity of SCCmec types and the existence of psm-mec in CNS isolates from CNS PD-related peritonitis. The current study demonstrated a high prevalence of MRCNS harboring SCCmec type genes. The majority of isolates were hospital-associated isolates. Furthermore, the 2 isolates with psm-mec positivity were MRCNS in the NBFG. The SCCmec typing system is the major marker for distinguishing between CA-MRSA and HA-MRSA. The frequent exposure of such patients to hospitals is the main risk factor. Hence, strategies must be applied to prevent the spread of such pathogens in both community and hospital environments. As a result, additional large scale and comprehensive studies are needed to define the SCCmec type distribution and to determine the molecular epidemiological characteristics of psm-mec and its possible role in hospital and community infection in particular species. Additionally, more CNS samples are needed.
Availability of data and materials
The datasets generated and analyzed during the current study are available from the corresponding author on reasonable request.
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We thank the staff at the microbiological routine laboratory of Haikou People’s Hospital Affiliated to Xiangya School of Medicine for the strains.
This resarch was supported by the Hainan Provincial Natural Science Foundation of China [grant number, 820RC785 and 822RC864] and the Healthy department of Hainan province [grant number, 22A200302 and 21A200441].
Ethics approval and consent to participate
This research was approved by the Ethics Committee of Haikou People’s Hospital [No. SC20190053]. Written informed consent was obtained from the patients. All methods were carried out in accordance with relevant regulations and guidelines.
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Zhou, J., Yang, C., Lei, W. et al. Identification and characterization of SCCmec typing with psm-mec positivity in staphylococci from patients with coagulase-negative staphylococci peritoneal dialysis-related peritonitis. BMC Microbiol 23, 267 (2023). https://doi.org/10.1186/s12866-023-03017-2