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Journal of Clinical Microbiology, October 2006, p. 3804-3807, Vol. 44, No. 10
0095-1137/06/$08.00+0     doi:10.1128/JCM.00395-06
Copyright © 2006, American Society for Microbiology. All Rights Reserved.

Comparison of PCR-Based Methods for Typing Staphylococcus aureus Isolates

Artur Sabat,1,{dagger} Natalia Malachowa,2,{dagger} Jacek Miedzobrodzki,2 and Waleria Hryniewicz1*

National Institute of Public Health, 00-725 Warsaw, Poland,1 Department of Microbiology, Faculty of Biotechnology, Jagiellonian University, 30-387 Cracow, Poland2

Received 22 February 2006/ Returned for modification 26 May 2006/ Accepted 7 July 2006


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ABSTRACT
 
In this study, we compared the potentials of (i) a multiplex PCR-based multilocus variable-number tandem repeat (VNTR) assay; (ii) a triplex PCR coamplifying fragments of spa, coa, and the hypervariable region adjacent to the mecA gene; (iii) restriction profile analysis of the STAR repetitive element; (iv) randomly amplified polymorphic DNA analysis; (v) inter-IS256 PCR; and (vi) rep-MP3 PCR. Multilocus VNTR typing and triplex PCR (coa, spa, and hypervariable region) approaches showed excellent reproducibility and high discriminatory power; however, only multilocus VNTR typing could distinguish all pulsed-field gel electrophoresis and spa types. Multilocus VNTR typing appears to be the most useful PCR-based method for the rapid genotyping of Staphylococcus aureus strains.


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TEXT
 
Staphylococcus aureus is an increasingly common cause of nosocomial and community-acquired infections worldwide. Therefore, the detection of outbreaks of staphylococcal infections, as well as the identification of "successful" clones with enhanced virulence or increased ability to spread epidemically, is essential. The traditional methods of S. aureus typing have largely been replaced by molecular typing systems. These fulfill all of the criteria required for usefulness, including performance (typeability, reproducibility, stability, and discriminatory power) and convenience (rapidity, accessibility, ease of use, and ease of interpretation) (14, 18). Individually, however, they may suffer from various shortfalls.

Among the methods for molecular typing of S. aureus isolates, pulsed-field gel electrophoresis (PFGE) is considered to be the gold standard. Unfortunately, this method is technically demanding and time-consuming. Moreover, achieving full reproducibility between laboratories is challenging, thus making data comparison difficult (22). However, successful efforts at intercenter standardization of protocols were achieved, therefore allowing the development of multicenter methicillin-resistant S. aureus (MRSA) surveillance networks (2, 12, 13).

Traditional PCR-based techniques, in comparison to PFGE, are easier, faster, and increasingly less expensive to perform but also have several limitations. In the cases of a randomly amplified polymorphic DNA (RAPD) assay and a repetitive element sequence-based PCR (rep-PCR) analysis, the major drawback relates to insufficient standardization and low laboratory-to-laboratory reproducibility (3, 21). The PCR-based locus-specific restriction fragment length polymorphism technique suffers from limited discriminatory power as was shown by coagulase gene analysis (1). Methods which utilize DNA sequencing, including multilocus sequence typing (MLST) (5) and spa typing (8, 10), have a good discriminatory power and full portability of data, but their cost is a limiting factor for most laboratories.

During the past few years, many efforts have been made to develop new PCR-based typing methods for S. aureus. Among these methods is a triplex PCR aimed to amplify fragments of spa, coa, and the hypervariable region adjacent to the mecA gene (HVR) (17, 24), as well as restriction profile analysis of the repetitive element called STAR (STAR-RP) (15). Recently, a multiplex PCR method for multiple-locus variable-number tandem repeat (VNTR) analysis (16) has been developed. In our previous publications, we called this method multiple-locus VNTR analysis, but in fact, this is a "fingerprinting" approach, since it does not allow an analysis of the exact number of repeats in the obtained amplification products and determining which band corresponds to which PCR target is impossible. The resulting data cannot be compared between different laboratories. Therefore, we would like to rename this method multiple-locus VNTR fingerprinting (MLVF). The simultaneous analysis of the variation in number of repeat units in seven individual genes (sspA, spa, sdrC, sdrD, sdrE, clfA, and clfB) endows MLVF with a discriminatory power comparable to PFGE (11). On the basis of PFGE interpretation rules by Tenover et al. (20), criteria for clustering MLVF patterns have been suggested (11). Isolates classified into the same MLVF cluster differing by up to six DNA fragments, among a maximum of 14 bands, differed by no more than 6 bands in PFGE analysis. However, outbreak analysis and short-time interhospital spread of a highly clonal organism such as S. aureus demand more stringent criteria in MLVF interpretation. In more stringent conditions, the MLVF clusters grouped isolates that differed by up to four bands, which reflected up to three bands of difference between two PFGE patterns. Recently, Francois and colleagues (6) automatized and expanded MLVF with additional virulence genes containing repeat units (fnbA, fnbB, and cna).

Recently developed PCR-based typing methods (MLVF, expanded MLVF, triplex PCR [coa, spa, and HVR], and STAR-RP) have been poorly evaluated in comparison to the well-established assays (RAPD PCR and rep-PCR). The new methods require careful assessment of their potential for typing S. aureus strains, and there is a need to identify the most efficient PCR approach. In this study, we therefore evaluated six PCR-based typing methods and compared the results with those obtained by Malachowa et al. (11).

Fifty-nine nosocomial S. aureus strains, mostly MRSA isolates (Table 1), were obtained from the collection previously characterized by PFGE, MLVF, MLST, and spa typing (11). All isolates were subjected to six different PCR-based typing techniques that included (i) the multiple-locus variable-number tandem repeat-based method (expanded MLVF) with a primer mix to simultaneously amplify the parts of genes coding for serine protease V8 (sspA), protein A (spa), Ser-Asp-rich fibrinogen-binding proteins (sdrCDE), clumping factor A (clfA), clumping factor B (clfB), fibronectin-binding proteins (fnbAB), and collagen adhesin A (cna); (ii) triplex PCR (coa, spa, and HVR) with a primer mix to simultaneously amplify a part of the coa gene (coding for coagulase), a part of the spa gene (coding for protein A), and the hypervariable region adjacent to the mecA gene (17, 24); (iii) STAR-RP (15); and (iv) RAPD using the combination of primers EP007 and KAY1 (19); as well as two different rep-PCR methods, (v) inter-IS256 (4) and (vi) rep-MP3 (23). The typing methods were performed with published protocols, with the exception of expanded MLVF, for which each PCR mixture was separated in 2% agarose Micropor GAMMA (Prona) gel by using a classical electrophoretic approach. Any two patterns produced by each of the six PCR genotyping procedures differing by one or more bands were considered distinct types. In order to test the reproducibilities of the PCR-based typing systems, we obtained the patterns from 20 isolates in three independent experiments with different DNA preparations. Reproducibility was defined as the ability to yield identical PCR patterns in testing the same isolate during different experiments. It was expressed as the percentage of isolates that gave the same profile in separate experiments. The discriminatory power of each PCR-based fingerprinting method was estimated by the number of identified patterns among 40 epidemiologically unrelated isolates (Table 1) and by Simpson's index of diversity (9). Ninety-five percent confidence intervals (CI95) for discriminatory indices were calculated as previously described (7). Nonoverlapping confidence intervals were regarded as indicating statistically significant differences in discriminatory power (7). The calculation of intermethod concordance was conducted as described before (11).


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  		TABLE 1. Origin, methicillin phenotype, and typing results for 59 S. aureus isolatesf

Fifty-nine isolates of S. aureus were typeable by all the methods used in this study. Analysis of reproducibility was further performed three times on the reextracted total DNA of 20 isolates. An excellent reproducibility (100%) was observed for the expanded MLVF, triplex PCR, and STAR-RP methods, whereas reproducibilities of inter-IS256 (85%), RAPD (80%), and rep-MP3 (75%) were lower. The intensity of the HVR amplicon in triplex PCR approach varied in different runs, but this, however, did not compromise the reproducibility of the method.

We further analyzed only those methods whose reproducibility was 100%. The expanded MLVF approach was the most discriminatory PCR-based method in this study, but in the case of triplex PCR, a difference was not statistically significant because of overlapping 95% confidence intervals (0.98 [CI95, 0.98 to 1.00] and 0.96 [CI95, 0.94 to 0.98]). The discriminatory power of STAR-RP was only 0.80 (CI95, 0.74 to 0.86), and STAR-RP differed substantially from other PCR typing methods tested. Expanded MLVF distinguished 34 patterns that exactly matched the 34 MLVF profiles obtained previously (11). None of the PCR methods tested was able to distinguish all of the epidemiologically unrelated isolates (Table 1). However, only expanded MLVF could distinguish all isolates with distinct PFGE types (from types A to Y). Also, expanded MLVF was the only method which could differentiate between all spa types. In other words, different PFGE or spa types translated into different MLVF patterns.

Concordance between the methods evaluated in this study ranged from 23.7 to 76.3% (Table 2), when all isolates from the collection were studied. The best concordances of results were found for spa typing with triplex PCR (76.3%) and MLST (72.9%) as well as expanded MLVF with PFGE (72.9%) and triplex PCR (71.2%). Overall, there was a high degree of concordance between the results obtained by the typing techniques with similar discriminatory abilities. In contrast, the least concordance values were observed between the typing methods which displayed different discriminative potentials, such as PFGE and STAR-RP (23.7%) or PFGE and MLST (32.2%).


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  		TABLE 2. Correlation between typing methods for S. aureus

Reproducibility is one of the most important parameters of any bacterial typing method. Among the PCR-based typing methods with high discriminatory power, expanded MLVF and triplex PCR had excellent reproducibilities (100%). Therefore, these approaches allow reliable comparisons across large numbers of assays and for comparing archived fingerprint patterns.

The triplex PCR and expanded MLVF approaches revealed very good concordances with spa typing, 76.3% and 62.7%, respectively. Both PCR methods utilize the VNTR region of the spa gene. Despite the fact that there was better concordance between triplex PCR and spa typing, only expanded MLVF could distinguish all spa types. Triplex PCR in some cases produced the same pattern for different spa types (triplex PCR types 1, 3, and 4). Moreover, better concordance was found between PFGE and expanded MLVF (72.9%) than between PFGE and triplex PCR (52.5%). Therefore, for large-scale surveillance, the MLVF methods are candidate screening tools for the identification of genetically identical isolates. From these, two or three representative isolates may be selected for further definitive characterization by spa typing in reference laboratories. The spa sequence data are unambiguous and electronically portable between laboratories. The searchable database on the Ridom SpaServer (www.ridom.de/spaserver), along with StaphType software (8), can be used to increase our knowledge of genetic and epidemiological data from various geographic regions. Therefore, the combined use of MLVF or expanded MLVF and spa typing can benefit the monitoring of hospital-to-hospital strain transmission events and public health interventions on a huge scale.

We demonstrated that among the methods based on PCR, MLVF and expanded MLVF are most effective for typing large collections of MRSA strains. MLVF methods fulfill all the criteria for broadly used typing techniques, so they are rapid and inexpensive and not labor-intensive, with excellent discriminatory power and reproducibility. Adequate concordances with other highly discriminative typing methods, such as PFGE and especially spa typing, enable the MLVF approaches to be valuable techniques with an application to the investigation of outbreaks and for epidemiological tracing of S. aureus.


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ACKNOWLEDGMENTS
 
These studies were supported by grants 2 P04A 001 27 (to A.S. and W.H.) and PBZ-KBN-101/T09/2003/14 (to J.M.) from the Committee of Scientific Research (KBN, Poland).

We thank Alex van Belkum (Erasmus MC University Medical Center, Rotterdam, The Netherlands) for revision of the manuscript.


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FOOTNOTES
 
* Corresponding author. Mailing address: National Institute of Public Health, 30/34 Chelmska St., 00-725 Warsaw, Poland. Phone: 48 22 841 33 67. Fax: 48 22 841 29 49. E-mail: waleria{at}cls.edu.pl. Back

{dagger} These authors contributed equally to this work. Back


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Journal of Clinical Microbiology, October 2006, p. 3804-3807, Vol. 44, No. 10
0095-1137/06/$08.00+0     doi:10.1128/JCM.00395-06
Copyright © 2006, American Society for Microbiology. All Rights Reserved.



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