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Year : 2016  |  Volume : 4  |  Issue : 1  |  Page : 2-8

Methicillin-Resistant Staphylococcus Aureus in Saudi Arabia: Genotypes distribution review

Department of Medical Laboratory Sciences, College of Applied Medical Sciences, University of Dammam, Hafr Al Batin, Saudi Arabia

Date of Web Publication2-Dec-2015

Correspondence Address:
Sulaiman A Al Yousef
Department of Medical Laboratory Sciences, College of Applied Medical Sciences, University of Dammam, P.O. Box 1683, Hafr Al Batin - 31991
Saudi Arabia
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DOI: 10.4103/1658-631X.170880

PMID: 30787687

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Methicillin-resistant Staphylococcus aureus (MRSA) infections in hospital have obviously imposed a significant burden of morbidity and mortality, and strain on healthcare resources. Here, we review the genotype distribution of these pathogens in the Kingdom of Saudi Arabia (KSA). A PubMed literature search (until May 2014) specified 12 articles that characterized MRSA clones in KSA. Only two regions (Riyadh and Damamm) were represented in ten articles. Data from these articles showed that the pandemic Vienna/Hungarian/Brazilian clone (CC8/ST239-III) is the most frequent in Saudi regions (Riyadh and Damamm). Several other clones such as Barnim/UK-EMRSA-15 (CC22-IV), Southwest Pacific clone (ST30-IV) and European community-associated-MRSA clone (CC80-IV) have been detected in the Riyadh region. A variety of MRSA clones is beginning to circulate in Saudi hospitals. Continued collection and molecular characterization of MRSA is crucial for the effective prevention and treatment.

  Abstract in Spanish 

ملخص البحث :

العدوى الناشئة عن البكتيريا العنقودية المقاومة للميثيسيلين في المستشفيات شكلت عبئاً كبيراً على موارد الرعاية الصحية بالإضافة إلى زيادة معدلات المرض والوفيات. يستعرض الباحثان توزيع الأنماط الجينية بين هذه الجراثيم في المملكة العربية السعودية. أجري البحث في قاعدة البيانات (PupMed) واستعرض الباحثان عشرة ابحاث منشورة لمنطقتي الرياض والدمام. وأظهرت المعلومات انتشار نسيله فيينا / المجر/ البرازيل بصورة وبائية في المملكة. وكذلك انتشار أعداد أخرى من النسائل في الرياض وهي بارنيم/ المملكة المتحدة وجنوب غرب المحيط الهادي والنسيلة الأوربية المكتسبة من المجتمع. يتضح من ذلك ان هناك العديد من النسائل لهذه البكتيريا العنقودية والتي بدأت في الانتشار في المستشفيات السعودية. الاستمرار الدائم في جمع والتوصيف الجزيئي لهذه البكتيريا العنقودية أمر بالغ الأهمية للوقاية والعلاج الفعال.

Keywords: Genotypes, methicillin-resistant Staphylococcus aureus, Saudi

How to cite this article:
Al Yousef SA, Taha EM. Methicillin-Resistant Staphylococcus Aureus in Saudi Arabia: Genotypes distribution review. Saudi J Med Med Sci 2016;4:2-8

How to cite this URL:
Al Yousef SA, Taha EM. Methicillin-Resistant Staphylococcus Aureus in Saudi Arabia: Genotypes distribution review. Saudi J Med Med Sci [serial online] 2016 [cited 2022 Jan 21];4:2-8. Available from: https://www.sjmms.net/text.asp?2016/4/1/2/170880

  Introduction Top

Methicillin-resistant Staphylococcus aureus (MRSA) infections represent a major challenge to hospital microbiologists because of the emergence and spread of clones that have decreased susceptibility to many antibiotic classes. [1],[2] Methicillin-resistance in staphylococci is due to the acquisition of one of the several staphylococcal cassette chromosomes (SCCmec), that carries a mec A gene that encodes a penicillin-binding protein conferring resistance to methicillin. [3] Molecular typing approaches have been used to great advantage in establishing clonal relationships between strains besides identifying and monitoring the international spread of some unique MRSA strains. [4],[5] A variety of molecular techniques has now been introduced for the study of the epidemiology of MRSA. [6] These include SCCmec typing, [7],[8],[9] pulse field gel electrophoresis (PFGE), [10] multilocus sequence typing (MLST), [11] and Staphylococcus protein A gene (spa) typing. [12],[13],[14] PFGE, MLST, and spa typing are the most widely used typing techniques because of their high discriminatory power and reproducibility. [15]

In Saudi studies, the prevalence of MRSA among S. aureus and temporal increases have been shown to vary widely among the regions. [16],[17] Recently, the overall estimation of the prevalence of MRSA in Saudi Arabia (KSA) was 35.6% from pooled estimation of 22,793 S. aureus strains from 2002 to 2012. [18]

The aim of the present review was to provide an overview of the genotypes present throughout Saudi Arabia to support the use of effective treatments and to guide strategies for the control of the spread of MRSA.

  Geography of KSA and Data Acquisition Top

KSA is one of the most populous countries and the largest in the Arabian Peninsula (2 × 10 6 Km 2 ). The population of KSA is estimated around 28 million, about 20% of whom are expatriates mainly from the Indian subcontinent and Southeast Asia. Moreover, KSA hosts more than 4 million Muslim pilgrims from across the globe during the Hajj and Umra seasons. [16],[19] Mass gathering of millions of Muslims for the Hajj from all over the world in the same region increases the possibility of infectious pathogens, especially MRSA strains. The above-mentioned conditions make KSA a hot spot for the collection of MRSA and its global spread.

For this review, we performed a literature search to evaluate the history and distribution of MRSA clones within KSA. We searched the PubMed/MEDLINE database of all published articles related to genotyping MRSA in Saudi Arabia until May 2014. Search terms (and combinations thereof) were: "MRSA clones," "'Methicillin resistant Staphylococcus aureus clones," "MRSA," "genetic," "molecular characterization," "typing," "genotypes," and "Saudi". Hand search of references listed in relevant articles was also carried out.

Most of the pertinent published data on genotyping MRSA came from only three regions out of a total of 13 regions in KSA. Only 12 relevant published articles reporting data collected were included: Nine from Riyadh (1998-2011), one from Dammam (2001-2003), one from Jeddah (2009-2011), and one from different cities in KSA (1992-1995). A variety of genotyping methods had been used to identify MRSA clones. Some studies applied only one technique (PFGE three articles and SCCmec three articles). Three other articles used two techniques (SCCmec and MLST). One article used PFGE and SCCmec; another study applied PFGE and MLST techniques; and one used three techniques (SCCmec, MLST, and spa) [Table 1].
Table 1: Distribution of MRSA isolates from Saudi regions by their genotypic characteristics until May 2014

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  Distribution of Methicillin-Resistant Staphylococcus Aureus Genotypes in KSA Top

The data collected in [Table 1] show that the earliest publication from KSA described the inter-hospital spread of a single MRSA clone between 1992 and 1995. Ninety-four strains of MRSA, originating from inpatients across geographically diverse regions of KSA were genetically typed by randomly amplified polymorphic DNA and a representative subset of the strains was analyzed by PFGE as well. However, 93% (87/94) of the isolates belonged to a single clonally related lineage of MRSA and seven other isolates differed only slightly from those determined for the clonal type. [20] Eight years later, in contrast to the Romania strains, MRSA strains collected from institutions in Dammam (n = 60) and Dhahran (n = 8) between April 2001 and May 2003 shared a common PFGE pattern and MLST (ST239). This indicated that a single epidemic clone was spreading in Saudi Arabia. The MRSA strains were differentiated using PFGE of sma I DNA macrorestriction fragments. A comparison of PFGE fingerprints identified clusters of strains with clear segregation branches according to the hospital they had originated from. However, MLST revealed that all strains except two (ST5 and ST254) shared the ST239 genotype. Even the relatively closed PFGE-based dendrogram indicated a diversity of ST239. [21]

Data based on evolutionary patterns and genotypic characteristics again indicated that a single epidemic clone of MRSA was widespread in Saudi Arabia compared with other Asian countries. In this review, five MRSA strains (from King Khalid University Hospital, Riyadh during 1998-2003 were analyzed by MLST and SCCmec typing. Data indicated that all five MRSA strains belonged to a single, epidemic clone ST241 (a single-locus variant of ST239) and CC239 with SCCmec IIIA. [22] A description of SCCmec elements carried by 19 MRSA strains isolated in King Khalid University Hospital, Riyadh, from 1998 to 1999 was reported. Eighteen MRSA strains were classified as SCCmec 3A (III) type, and the frequency of type SCCmec 2B (IV) was very low (1/19). Subsequently, the genotypes of representative five isolates were investigated by MLST. The dominant four MRSA strains belonged to CC8 (ST239), and one minor strain of CC5 (ST5) were reported. [23]

Although one MRSA clone is widespread in KSA, other clones are also beginning to spread. Baddour et al. performed comparative chromosomal DNA analysis of 512 MRSA strains from seven hospitals in Riyadh between 2004 and 2005 using PFGE. They were categorized into six major PFGE patterns (M1-M6), and M1 was numerically predominant and widespread (187 strains, 36.5%) followed by an M2 type (105 strains, 20.5%). Unique PFGE type was designated and reported as a prevalent pattern (84 strains, 16.4%). [24] In the same way, three major clusters were revealed from the 30 MRSA strains collected from major hospital laboratories and public health centers in Riyadh in 2009 and typed by using PFGE. The first, which included 17 strains were subdivided into four groups, and the second consisted of 12 strains, while the third cluster contained only one strain. [25]

Other MRSA strains have been described with genes encoding Panton-Valentine leukocidin (PVL), harboring SCCmec type IV-traits that are usually associated with community-associated methicillin-resistant Staphylococcus aureus (CA-MRSA). MRSA genotyping data showed a much lower PVL prevalence of only 8% (three out of 37) in SCCmec IV strains from outpatient clinics in King Khalid University Hospital, Riyadh, in 2007. [26] In another report, Moussa and Hessan found that only 18 strains (13.33%) recovered from skin and soft tissue infections were positive for PVL and (SCCmec) type IV. [27] Furthermore, in an investigation of a CA-MRSA outbreak among healthy neonates at a tertiary care teaching hospital in Riyadh between October and November 2009, 10 MRSA isolates (nine infants and one mother) were characterized using PFGE and SCCmec typing. Although all 10 MRSA isolates harbored SCCmec IV type, nine MRSA were of the same PFGE pattern but the remaining one was different. [28] Recently, 101 clinical isolates of MRSA, taken from a Jeddah Hospital and Health Centers from August 2009 to May 2011, were investigated genetically by SCCmec typing and genes encoding PVL. SCCmec III (39 strains) were the most predominant type. Only 38 strains (37.6%) harbored PVL gene while SCCmec V (43 strains). Some minor strains belonged to SCCmec IVa and IVc (16 and 3 strains, respectively), but no SCCmec types I, II, IVb or IVd were detected. [29]

The first MRSA typing data from Saudi Arabia were obtained by Monecke et al. When 107 MRSA isolates from King Fahad Medical City in Riyadh between summer 2010 and spring 2011 were characterized by DNA microarrays, the most predominant five MRSA strains from four clonal complexes found were CC8/ST239-III (Vienna/Hungary/Brazil Epidemic strain-20.75%) PVL-positive, and negative CC22-IV (UK-EMRSA-15/Barnim Epidemic strain-18.87% and 9.43%, respectively), PVL-positive CC30-IV (Southwest Pacific clone-12.26%) and PVL-positive CC80-IV (European CA-MRSA clone-17.92%). Other strains which accounted for <3% each included PVL-negative CC5-IV, CC5-IV/SCCfus, CC6-IV (West Australian, WA, MRSA-51/66) and PVL-positive CC88-IV, PVL-positive CC5-IV, PVL-positive CC80-IV, CC97-V as well as CC1-IV/SCCfus (WA MRSA-1/45), PVL-positive CC1/ST772-V (Bengal Bay clone/WA MRSA-60), PVL-negative CC5-V, CC45-IV (WA MRSA-23), and a CC9/ST834-MRSA strain with an identified SCCmec element. Surprisingly, the prevalence of PVL genes was significantly higher (54.21%). [30] Alreshidi et al. provided the first data on MRSA genotypes and virulence gene profiles in cancer patients. A total of 120 MRSA isolates from cancer and noncancer patients in the Armed Forces Hospital in Riyadh in February and August 2010, were investigated using SCCmec, MLST, spa, and virulence genes detection. SCCmec type III was detected in all MRSA isolates, but no PVL gene was detected. According to spa typing, MRSA strains were clustered into six groups including cluster-1 spa CC 037 (66 strains), cluster 3 spa CC 376 (25 strains), cluster 2 spa CC 790 (9 strain) as well as some minor clusters. Four novel spa types (local spa types) were detected and identified as t7604, t8506, t8507, and t8855. MRSA strains were classified into two different clonal clusters and three singletons. Group-1 including ST239 (70 strains), ST08 (seven strains), and ST241 (three strains) was the most prevalent followed by group-2 (ST22 and ST217) and five minor singleton groups (ST182, ST71, ST88, ST30, and ST80,). [31]

  Predominant Methicillin-Resistant Staphylococcus Aureus Clones in KSA Top

Although few published data about MRSA genotyping in KSA (12 published papers) are available, what are presented above give an overview of the genotyping of MRSA currently circulating in KSA and allow a comparison to be made with other countries. In this review, we found that the pandemic Vienna/Hungarian/Brazilian clone (CC8/ST239-III) and its variants continue to circulate in Dammam and Riyadh. ST239-III, mainly hospital-associated was the largest group detected in most studies from 2001 to 2013. Another clone, the pediatric clone (CC5), has been found in KSA hospitals though cases are rare. In recent years (2012-2013), many diverse strains of MRSA have been identified in the Riyadh region. Besides the Vienna/Hungarian/Brazilian and pediatric clones disseminated in KSA, several other common clones have also been identified. Barnim/UK-EMRSA-15 (CC22-IV), Southwest Pacific clone (ST30-IV), and European CA-MRSA clone (CC80-IV) are the most common clones in Riyadh hospitals [Figure 1].
Figure 1: Distribution of most predominant Methicillin-resistant Staphylococcus aureus clones in Saudi regions

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  References Top

Okesola AO. Community-acquired methicillin-resistant Staphylococcus aureus - A review of literature. Afr J Med Med Sci 2011;40:97-107.  Back to cited text no. 1
Jevons MP, Coe AW, Parker MT. Methicillin resistance in staphylococci. Lancet 1963;1:904-7.  Back to cited text no. 2
Rodríguez-Noriega E, Seas C, Guzmán-Blanco M, Mejía C, Alvarez C, Bavestrello L, et al. Evolution of methicillin-resistant Staphylococcus aureus clones in Latin America. Int J Infect Dis 2010;14:e560-6.  Back to cited text no. 3
Murchan S, Kaufmann ME, Deplano A, de Ryck R, Struelens M, Zinn CE, et al. Harmonization of pulsed-field gel electrophoresis protocols for epidemiological typing of strains of methicillin-resistant Staphylococcus aureus: A single approach developed by consensus in 10 European laboratories and its application for tracing the spread of related strains. J Clin Microbiol 2003;41:1574-85.  Back to cited text no. 4
Shittu A, Nübel U, Udo E, Lin J, Gaogakwe S. Characterization of meticillin-resistant Staphylococcus aureus isolates from hospitals in KwaZulu-Natal province, Republic of South Africa. J Med Microbiol 2009;58:1219-26.  Back to cited text no. 5
Aires de Sousa M, de Lencastre H. Bridges from hospitals to the laboratory: Genetic portraits of methicillin-resistant Staphylococcus aureus clones. FEMS Immunol Med Microbiol 2004 8;40:101-11.  Back to cited text no. 6
International Working Group on the Classification of Staphylococcal Cassette Chromosome Elements (IWG-SCC). Classification of staphylococcal cassette chromosome mec (SCCmec): Guidelines for reporting novel SCCmec elements. Antimicrob Agents Chemother 2009;53:4961-7.  Back to cited text no. 7
García-Álvarez L, Holden MT, Lindsay H, Webb CR, Brown DF, Curran MD, et al. Meticillin-resistant Staphylococcus aureus with a novel mecA homologue in human and bovine populations in the UK and Denmark: A descriptive study. Lancet Infect Dis 2011;11:595-603.  Back to cited text no. 8
Li S, Skov RL, Han X, Larsen AR, Larsen J, Sørum M, et al. Novel types of staphylococcal cassette chromosome mec elements identified in clonal complex 398 methicillin-resistant Staphylococcus aureus strains. Antimicrob Agents Chemother 2011;55:3046-50.  Back to cited text no. 9
Tenover FC, Arbeit RD, Goering RV, Mickelsen PA, Murray BE, Persing DH, et al. Interpreting chromosomal DNA restriction patterns produced by pulsed-field gel electrophoresis: Criteria for bacterial strain typing. J Clin Microbiol 1995;33:2233-9.  Back to cited text no. 10
Deurenberg RH, Vin C, Kalenic S, Friedrich AW, Bruggeman CA, Stobberingh EE. The molecular evolution of methicillin-resistant Staphylococcus aureus. Clin Microbiol Infect 2007;13:222-35.  Back to cited text no. 11
Frénay HM, Bunschoten AE, Schouls LM, van Leeuwen WJ, Vandenbroucke-Grauls CM, Verhoef J, et al. Molecular typing of methicillin-resistant Staphylococcus aureus on the basis of protein A gene polymorphism. Eur J Clin Microbiol Infect Dis 1996;15:60-4.  Back to cited text no. 12
Shopsin B, Gomez M, Montgomery SO, Smith DH, Waddington M, Dodge DE, et al. Evaluation of protein A gene polymorphic region DNA sequencing for typing of Staphylococcus aureus strains. J Clin Microbiol 1999;37:3556-63.  Back to cited text no. 13
Kahl BC, Mellmann A, Deiwick S, Peters G, Harmsen D. Variation of the polymorphic region X of the protein A gene during persistent airway infection of cystic fibrosis patients reflects two independent mechanisms of genetic change in Staphylococcus aureus. J Clin Microbiol 2005;43:502-5.  Back to cited text no. 14
Al-Zahrani IA, Hamson C, Edge D, Collins J, Perry JD, Raza M, et al. SmaI restriction site-based multiplex PCR for typing of hospital- and community-acquired Staphylococcus aureus. J Clin Microbiol 2011;49:3820-8.  Back to cited text no. 15
Yezli S, Shibl AM, Livermore DM, Memish ZA. Antimicrobial resistance among Gram-positive pathogens in Saudi Arabia. J Chemother 2012;24:125-36.  Back to cited text no. 16
Aly M, Balkhy HH. The prevalence of antimicrobial resistance in clinical isolates from Gulf Corporation Council countries. Antimicrob Resist Infect Control 2012;1:26.  Back to cited text no. 17
Al-Yousef SA, Mahmoud SY, Taha EM. Prevalence of methicillin-resistant Staphylococcus aureus in Saudi Arabia: Systemic review and meta-analysis. Afr J Clin Exp Microbiol 2013;14:146-54.  Back to cited text no. 18
Shibl A, Senok A, Memish Z. Infectious diseases in the Arabian Peninsula and Egypt. Clin Microbiol Infect 2012;18:1068-80.  Back to cited text no. 19
Van Belkum A, Vandenbergh M, Kessie G, Qadri SM, Lee G, van den Braak N, et al. Genetic homogeneity among methicillin-resistant Staphylococcus aureus strains from Saudi Arabia. Microb Drug Resist 1997;3:365-9.  Back to cited text no. 20
Cîrlan M, Saad M, Coman G, Bilal NE, Elbashier AM, Kreft D, et al. International spread of major clones of methicillin resistant Staphylococcus aureus: Nosocomial endemicity of multi locus sequence type 239 in Saudi Arabia and Romania. Infect Genet Evol 2005;5:335-9.  Back to cited text no. 21
Ko KS, Lee JY, Suh JY, Oh WS, Peck KR, Lee NY, et al. Distribution of major genotypes among methicillin-resistant Staphylococcus aureus clones in Asian countries. J Clin Microbiol 2005;43:421-6.  Back to cited text no. 22
Chongtrakool P, Ito T, Ma XX, Kondo Y, Trakulsomboon S, Tiensasitorn C, et al. Staphylococcal cassette chromosome mec (SCCmec) typing of methicillin-resistant Staphylococcus aureus strains isolated in 11 Asian countries: A proposal for a new nomenclature for SCCmec elements. Antimicrob Agents Chemother 2006;50:1001-12.  Back to cited text no. 23
Baddour MM, Abuelkheir MM, Fatani AJ, Bohol MF, Al-Ahdal MN. Molecular epidemiology of methicillin-resistant Staphylococcus aureus (MRSA) isolates from major hospitals in Riyadh, Saudi Arabia. Can J Microbiol 2007;53:931-6.  Back to cited text no. 24
Moussa IM, Al-Qahtani AA, Gassem MA, Ashgan MH, Ismail DK, Ghazy AI, et al. Pulsed-field gel electrophoresis (PFGE) as an epidemiological marker for typing of methicillin resistant Staphylococcus aureus recovered from KSA. Afr J Microbiol Res 2011;5:1492-9.  Back to cited text no. 25
Moussa I, Shibl AM. Molecular characterization of methicillin-resistant Staphylococcus aureus recovered from outpatient clinics in Riyadh, Saudi Arabia. Saudi Med J 2009;30:611-7.  Back to cited text no. 26
Moussa IM, Hessan AM. Rapid detection of community acquired-methicillin resistance Staphylococcus aureus recovered from King Saudi Arabia. Afr J Microbiol Res 2010;4:2804-10.  Back to cited text no. 27
Alsubaie S, Bahkali K, Somily AM, Alzamil F, Alrabiaah A, Alaska A, et al. Nosocomial transmission of community-acquired methicillin-resistant Staphylococcus aureus in a well-infant nursery of a teaching hospital. Pediatr Int 2012;54:786-92.  Back to cited text no. 28
Moussa I, Kabli SA, Hemeg HA, Al-Garni SM, Shibl AM. A novel multiplex PCR for molecular characterization of methicillin resistant Staphylococcus aureus recovered from Jeddah, Kingdom of Saudi Arabia. Indian J Med Microbiol 2012;30:296-301.  Back to cited text no. 29
[PUBMED]  Medknow Journal  
Monecke S, Skakni L, Hasan R, Ruppelt A, Ghazal SS, Hakawi A, et al. Characterisation of MRSA strains isolated from patients in a hospital in Riyadh, Kingdom of Saudi Arabia. BMC Microbiol 2012;12:146.  Back to cited text no. 30
Alreshidi MA, Alsalamah AA, Hamat RA, Neela V, Alshrari AS, Atshan SS, et al. Genetic variation among methicillin-resistant Staphylococcus aureus isolates from cancer patients in Saudi Arabia. Eur J Clin Microbiol Infect Dis 2013;32:755-61.  Back to cited text no. 31


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