Diversity of <em>Spa</em> gene between methicillin-resistant and methicillin-sensitive <em>Staphylococcus aureus</em> bacteria in a tertiary referral hospital, Indonesia

  • Sri Amelia Department of Microbiology, Faculty of Medicine, Universitas Sumatera Utara, Medan, Indonesia https://orcid.org/0000-0001-5864-5926
  • R. Lia Kusumawati Department of Microbiology, Faculty of Medicine, Universitas Sumatera Utara, Medan, Indonesia https://orcid.org/0000-0002-0459-1026
  • Ridwan Balatif Faculty of Medicine, Universitas Sumatera Utara, Medan, Indonesia https://orcid.org/0000-0002-6638-3900
  • Tryna Tania Whole Genome Sequence Laboratory, Department of Microbiology, Faculty of Medicine, Universitas Sumatera Utara, Medan, Indonesia
  • Lavarina Winda Biomolecular Laboratory, Faculty of Medicine, Universitas Sumatera Utara, Medan, Indonesia
  • Nadya Adlin Syamira Department of Biotechnology, Faculty of Science and Mathematics, Universitas Diponegoro, Semarang, Indonesia
Keywords: bacterial typing techniques, Staphylococcus aureus, tertiary referral hospital


BACKGROUND Spa typing is an effective and fast technique to identify the prevalence and spread of Staphylococcus aureus strains based on their spa gene profiles. The distribution of spa types will contribute to control the spread of S. aureus. Little is known regarding the spa types of S. aureus in Indonesia. This study aimed to investigate the diversity of spa gene among S. aureus carriage isolates in North Sumatra Province, Indonesia.

METHODS 79 S. aureus isolates consisting of 39 methicillin-resistant S. aureus (MRSA) and 40 methicillin-susceptible S. aureus (MSSA) carriage isolates were identified by VITEK2 Compact (Biomerieux, Indonesia) to detect mecA gene. All samples underwent spa typing and sequencing.

RESULTS Spa gene was detected among 31/39 (79%) of the MRSA isolates and 24/40 (60%) of the MSSA isolates. Most spa typing genes were identified between 350 and 400 base pair (bp). t258 and t852 were the most prevalence spa types among MRSA and MSSA isolates, respectively.

CONCLUSIONS Many MRSA and MSSA isolates encoded spa gene. The most genes detected were t258 and t852, identified in Germany and Portugal, respectively; while t18977 was initially identified in Malaysia. This indicated a global spread of MRSA according to spa typing.


Taylor TA, Unakal CG. Staphylococcus aureus infection. [Updated 2022 Jul 18]. In: StatPearls. Treasure Island (FL): StatPearls Publishing; 2023.

Antimicrobial Resistance Collaborators. Global burden of bacterial antimicrobial resistance in 2019: a systematic analysis. Lancet. 2022;399(10325):629-55. https://doi.org/10.1016/S0140-6736(21)02724-0

Kuntaman K, Hadi U, Setiawan F, Koendori EB, Rusli M, Santosaningsih D, et al. Prevalence of methicillin resistant Staphylococcus aureus from nose and throat of patients on admission to medical wards of Dr Soetomo Hospital, Surabaya, Indonesia. Southeast Asian J Trop Med Public Health. 2016;47(1):66-70.

Arcenas RC. Molecular methods for healthcare-acquired infections. In: Coleman WB, Tsongalis GJ. Diagnostic molecular pathology: a guide to applied molecular testing. New York: Academic Press; 2017. https://doi.org/10.1016/B978-0-12-800886-7.00014-5

Hakimi Alni R, Mohammadzadeh A, Mahmoodi P. Molecular typing of Staphylococcus aureus of different origins based on the polymorphism of the spa gene: characterization of a novel spa type. 3 Biotech. 2018;8(1):58. https://doi.org/10.1007/s13205-017-1061-6

Amelia S, Wahyuni DD, Yunita R, Rozi MF. The active surveillance of Staphylococcus aureus using polymerase chain reaction-based identification method among hospitalized-patient of Haji Adam Malik General Hospital, Medan, Indonesia. Open Access Maced J Med Sci. 2021;9(A): 622-5. https://doi.org/10.3889/oamjms.2021.6646

Harmsen D, Claus H, Witte W, Rothgänger J, Claus H, Turnwald D, et al. Typing of methicillin-resistant Staphylococcus aureus in a university hospital setting by using novel software for spa repeat determination and database management. J Clin Microbiol. 2003;41(12):5442-8. https://doi.org/10.1128/JCM.41.12.5442-5448.2003

Ridom SpaServer. SpaServer database [Internet]. Ridom GmbH; [cited 2022 Dec 2022]. Available from: https://spa.ridom.de/index.shtml.

Kareem SM, Aljubori SS, Ali MR. Novel determination of spa gene diversity and its molecular typing among Staphylococcus aureus Iraqi isolates obtained from different clinical samples. New Microbes New Infect. 2020;34:100653. https://doi.org/10.1016/j.nmni.2020.100653

Mohammed KAS, Abdulkareem ZH, Alzaalan AR, Yaqoob AK. Spa typing of Staphylococcus aureus isolated from clinical specimens from outpatients in Iraq. Pol J Microbiol. 2021;70(1):79-85. https://doi.org/10.33073/pjm-2021-007

Shakeri F, Shojai A, Golalipour M, Rahimi Alang S, Vaez H, Ghaemi EA. Spa diversity among MRSA and MSSA strains of Staphylococcus aureus in North of Iran. Int J Microbiol. 2010;2010:351397. https://doi.org/10.1155/2010/351397

Omidi M, Firoozeh F, Saffari M, Sedaghat H, Zibaei M, Khaledi A. Ability of biofilm production and molecular analysis of spa and ica genes among clinical isolates of methicillin-resistant Staphylococcus aureus. BMC Res Notes. 2020;13(1):19. https://doi.org/10.1186/s13104-020-4885-9

Jones SU, Chua KH, Chew CH, Yeo CC, Abdullah FH, Othman N, et al. spa diversity of methicillin-resistant and -susceptible Staphylococcus aureus in clinical strains from Malaysia: a high prevalence of invasive European spa-type t032. PeerJ. 2021;9:e11195. https://doi.org/10.7717/peerj.11195

Baum C, Haslinger-Löffler B, Westh H, Boye K, Peters G, Neumann C, et al. Non-spa-typeable clinical Staphylococcus aureus strains are naturally occurring protein A mutants. J Clin Microbiol. 2009;47(11):3624-9. https://doi.org/10.1128/JCM.00941-09

Votintseva AA, Fung R, Miller RR, Knox K, Godwin H, Wyllie DH, et al. Prevalence of Staphylococcus aureus protein A (spa) mutants in the community and hospitals in Oxfordshire. BMC Microbiol. 2014;14:63. https://doi.org/10.1186/1471-2180-14-63

Deurenberg RH, Beisser PS, Visschers MJ, Driessen C, Stobberingh EE. Molecular typing of methicillin-susceptible Staphylococcus aureus isolates collected in the Yogyakarta area in Indonesia, 2006. Clin Microbiol Infect. 2010;16(1):92-4. https://doi.org/10.1111/j.1469-0691.2009.02799.x

Zukancic A, Khan MA, Gurmen SJ, Gliniecki QM, Moritz-Kinkade DL, Maddox CW, et al. Staphylococcal protein A (spa) locus is a hot spot for recombination and horizontal gene transfer in Staphylococcus pseudintermedius. mSphere. 2020;5(5):e00666-20. https://doi.org/10.1128/mSphere.00666-20

Asadollahi P, Farahani NN, Mirzaii M, Khoramrooz SS, van Belkum A, Asadollahi K, et al. Distribution of the most prevalent Spa types among clinical isolates of methicillin-resistant and -susceptible Staphylococcus aureus around the world: a review. Front Microbiol. 2018;9:163. https://doi.org/10.3389/fmicb.2018.00163

Nübel U, Roumagnac P, Feldkamp M, Song JH, Ko KS, Huang YC, et al. Frequent emergence and limited geographic dispersal of methicillin-resistant Staphylococcus aureus. Proc Natl Acad Sci USA. 2008;105(37):14130-5.


Brignoli T, Manetti AGO, Rosini R, Haag AF, Scarlato V, Bagnoli F, et al. Absence of protein A expression is associated with higher capsule production in Staphylococcal isolates. Front Microbiol. 2019;10:863. https://doi.org/10.3389/fmicb.2019.00863

Hong X, Qin J, Li T, Dai Y, Wang Y, Liu Q, et al. Staphylococcal protein A promotes colonization and immune evasion of the epidemic healthcare-associated MRSA ST239. Front Microbiol. 2016;7:951. https://doi.org/10.3389/fmicb.2016.00951

Monaco M, Pimentel de Araujo F, Cruciani M, Coccia EM, Pantosti A. Worldwide epidemiology and antibiotic resistance of Staphylococcus aureus. Curr Top Microbiol Immunol. 2017;409:21-56. https://doi.org/10.1007/82_2016_3

How to Cite
Amelia S, Kusumawati RL, Balatif R, Tania T, Winda L, Syamira NA. Diversity of <em>Spa</em> gene between methicillin-resistant and methicillin-sensitive <em>Staphylococcus aureus</em&gt; bacteria in a tertiary referral hospital, Indonesia. Med J Indones [Internet]. 2023Aug.25 [cited 2024Feb.21];32(2):75-9. Available from: http://mji.ui.ac.id/journal/index.php/mji/article/view/6862
Basic Medical Research