Community-Acquired Methicillin-Resistant Staphylococcus aureus in Hospitals: Age-Specificity and Potential Zoonotic–Zooanthroponotic Transmission Dynamics

Methicillin-resistant Staphylococcus aureus (MRSA) lineages are a devastating clinical and public health issue. Data on local lineage profiles are limited. We report on the frequency of community-acquired and hospital-acquired cases (CA-MRSA, HA-MRSA). We studied 147 isolates from King Khalid tertiary care hospitals (KKH), each from a case in a patient and including 33 patients at the Maternity and Children’s Hospital (MCH). Of the 147 isolates, 87 males (59%) and 60 females (41%) were in KKH. The overwhelming majority (80%; n = 119/147) were CA-MRSA in KKH. Intriguingly, despite significant differences between males (70%) and females (53%), lineage-acquisition remained age-specific around 58–60 years in both genders. However, while CA-MRSA dominated early in life (0–20, 70% MCH), it increased with age in KKH adults; 21–50 (28%), >50 (59%) until the overall 80% (n = 144/180). Major specimens included skin-wounds, surgeries (70.3%), blood (13.5%), sputum (8.8%), very rarely urine (4.1%), and nasal (3.4%), albeit most patients showed severe enteritis and necrotizing pneumonia. Antibiograms showed high beta lactam resistances, including amoxicillin–clavulanate (83%), oxacillin (84%), cefoxitin FOX (100%), penicillin and ampicillin (~100%), as well as high resistance (82%) to carbapenem. Fortunately, high susceptibility was seen to non-beta lactams and, to a lesser extent, gentamicin, erythromycin, and fusidic acid; 33%, 34%, and 38%, respectively, in KKH. A similar pattern was seen in MCH except for a low resistance pattern to gentamicin CN, clindamycin CD, erythromycin E, and tobramycin TOB; 34%, 31%, 39%, and 41%, respectively, except for fusidic acid. These findings have significant clinical implications for MRSA patient management strategies. Clinical- and lineage-profiles imply host-selection and zoonotic–zooanthroponotic transmission dynamics. Future molecular typing, sequencing, and characterization of dominant clone(s) is imperative.

[1]  Mia Yang Ang,et al.  Diversity and Dissemination of Methicillin-Resistant Staphylococcus aureus (MRSA) Genotypes in Southeast Asia , 2022, Tropical medicine and infectious disease.

[2]  A. Abdollahi,et al.  Antimicrobial susceptibility testing of Staphylococcus aureus isolates from patients at a tertiary hospital in Tehran, Iran, 2018–2019 , 2022, European Journal of Medical Research.

[3]  E. El-Masry,et al.  MRSA as an indicator of infection control measures in Turaif General Hospital, Northern Area-Saudi Arabia. , 2022, Journal of infection in developing countries.

[4]  M. Shahid,et al.  Trends in methicillin-resistant Staphylococcus aureus in the Gulf Cooperation Council countries: antibiotic resistance, virulence factors and emerging strains. , 2022, Eastern Mediterranean health journal = La revue de sante de la Mediterranee orientale = al-Majallah al-sihhiyah li-sharq al-mutawassit.

[5]  Aisha Alamri,et al.  Eleven-Year surveillance of methicillin-resistant Staphylococcus aureus infections at an Academic Health Centre , 2022, Journal of preventive medicine and hygiene.

[6]  H. Iwasaki,et al.  Association of methicillin resistance with mortality of hospital-acquired Staphylococcus aureus bacteremia , 2021, The Journal of international medical research.

[7]  Rhys A. Farrer,et al.  Drivers of methicillin-resistant Staphylococcus aureus (MRSA) lineage replacement in China , 2021, Genome Medicine.

[8]  R. Amachawadi,et al.  Prevalence of Methicillin-resistant Staphylococcus Aureus in India: A Systematic Review and Meta-analysis , 2021, Oman medical journal.

[9]  A. Farhadi,et al.  Emergence of Highly Multidrug-Resistant Bacteria Isolated from Patients with Infections Admitted to Public Hospitals in Southwest Iran , 2021, Interdisciplinary perspectives on infectious diseases.

[10]  A. Salami,et al.  Prevalence, Laboratory Findings and Clinical Characteristics of Campylobacteriosis Agents among Hospitalized Children with Acute Gastroenteritis in Lebanon , 2021, Pediatric gastroenterology, hepatology & nutrition.

[11]  Gordon Y C Cheung,et al.  Pathogenicity and virulence of Staphylococcus aureus , 2021, Virulence.

[12]  S. Monecke,et al.  Genotyping of methicillin resistant Staphylococcus aureus from the United Arab Emirates , 2020, Scientific Reports.

[13]  G. Batiha,et al.  Methicillin-Resistant Staphylococcus aureus (MRSA): One Health Perspective Approach to the Bacterium Epidemiology, Virulence Factors, Antibiotic-Resistance, and Zoonotic Impact , 2020, Infection and drug resistance.

[14]  W. Alfouzan,et al.  Molecular Characterization of Methicillin- Resistant Staphylococcus aureus in a Tertiary Care hospital in Kuwait , 2019, Scientific Reports.

[15]  M. Khojasteh,et al.  Prevalence of and risk factors for methicillin-resistant Staphylococcus aureus nasal carriage in the West of Iran: a population-based cross-sectional study , 2019, BMC Infectious Diseases.

[16]  S. Monecke,et al.  Emergence of novel methicillin-resistant Staphylococcus aureus strains in a tertiary care facility in Riyadh, Saudi Arabia , 2019, Infection and drug resistance.

[17]  Yifan Rao,et al.  β-Lactam Antibiotics Enhance the Pathogenicity of Methicillin-Resistant Staphylococcus aureus via SarA-Controlled Lipoprotein-Like Cluster Expression , 2019, mBio.

[18]  E. Rutebemberwa,et al.  CA-MRSA and HA-MRSA coexist in community and hospital settings in Uganda , 2019, Antimicrobial Resistance & Infection Control.

[19]  J. Penadés,et al.  Staphylococcus aureus in Animals , 2019, Microbiology spectrum.

[20]  Islam M. Ghazi,et al.  Exploring bacterial resistance in Northern Oman, a foundation for implementing evidence-based antimicrobial stewardship program. , 2019, International journal of infectious diseases : IJID : official publication of the International Society for Infectious Diseases.

[21]  B. Sharma-Kuinkel,et al.  Methicillin-resistant Staphylococcus aureus: an overview of basic and clinical research , 2019, Nature Reviews Microbiology.

[22]  B. Allegranzi,et al.  Antimicrobial resistance: A round table discussion on the "One Health" concept from the Gulf Cooperation Council Countries. Part Two: A focus on Human Health. , 2018, Journal of infection and public health.

[23]  H. Chambers,et al.  PBP4: A New Perspective on Staphylococcus aureus β-Lactam Resistance , 2018, Microorganisms.

[24]  S. Foster,et al.  Staphylococcus aureus infection dynamics , 2018, PLoS pathogens.

[25]  Rania M. Seliem,et al.  Methicillin resistant Staphylococcus Aureus in emergency department patients in the United Arab Emirates , 2018, BMC Emergency Medicine.

[26]  S. Monecke,et al.  Emerging variants of methicillin-resistant Staphylococcus aureus genotypes in Kuwait hospitals , 2018, PloS one.

[27]  A. Al-Ali,et al.  Comparative and molecular analysis of MRSA isolates from infection sites and carrier colonization sites , 2018, Annals of Clinical Microbiology and Antimicrobials.

[28]  P. Linden,et al.  Incidence, prevalence, and management of MRSA bacteremia across patient populations—a review of recent developments in MRSA management and treatment , 2017, Critical Care.

[29]  A. Dashti,et al.  Characterization of Heterogeneous MRSA and MSSA with Reduced Susceptibility to Chlorhexidine in Kuwaiti Hospitals , 2017, Front. Microbiol..

[30]  N. H. Jazani,et al.  Methicillin‐resistant Staphylococcus aureus nasal carriage between healthy students of medical and nonmedical universities , 2017, American journal of infection control.

[31]  R. Isberg,et al.  Interplay Between Antibiotic Resistance and Virulence During Disease Promoted by Multidrug-Resistant Bacteria , 2017, The Journal of infectious diseases.

[32]  D. Pittet,et al.  The strategic plan for combating antimicrobial resistance in Gulf Cooperation Council States. , 2016, Journal of infection and public health.

[33]  Vance G. Fowler,et al.  Staphylococcus aureus Infections: Epidemiology, Pathophysiology, Clinical Manifestations, and Management , 2015, Clinical Microbiology Reviews.

[34]  A. Khalifa,et al.  Phenotypic and molecular characterization of HA-MRSA in Taif hospitals, Saudi Arabia. , 2015, Journal of infection in developing countries.

[35]  Edet E Udo Community-Acquired Methicillin-Resistant Staphylococcus aureus: The New Face of an Old Foe? , 2013, Medical Principles and Practice.

[36]  J. van der Palen,et al.  Emergence of Colistin Resistance in Enterobacteriaceae after the Introduction of Selective Digestive Tract Decontamination in an Intensive Care Unit , 2013, Antimicrobial Agents and Chemotherapy.

[37]  Tatsuo Yamamoto,et al.  Genetic nature and virulence of community-associated methicillin-resistant Staphylococcus aureus , 2013 .

[38]  H. Faidah,et al.  Methicillin-resistant Staphylococcus aureus in the western region of Saudi Arabia: prevalence and antibiotic susceptibility pattern , 2012, Annals of Saudi medicine.

[39]  S. Monecke,et al.  Characterisation of MRSA strains isolated from patients in a hospital in Riyadh, Kingdom of Saudi Arabia , 2012, BMC Microbiology.

[40]  Peter Donnelly,et al.  Evolutionary dynamics of Staphylococcus aureus during progression from carriage to disease , 2012, Proceedings of the National Academy of Sciences.

[41]  M. Falagas,et al.  Multidrug-resistant, extensively drug-resistant and pandrug-resistant bacteria: an international expert proposal for interim standard definitions for acquired resistance. , 2012, Clinical microbiology and infection : the official publication of the European Society of Clinical Microbiology and Infectious Diseases.

[42]  N. Akawi,et al.  Change in meticillin-resistant Staphylococcus aureus clones at a tertiary care hospital in the United Arab Emirates over a 5-year period , 2011, Journal of Clinical Pathology.

[43]  O. Sakwinska,et al.  Staphylococcus aureus Host Range and Human-Bovine Host Shift , 2011, Applied and Environmental Microbiology.

[44]  R. Guharoy,et al.  Penicillins , 2010, BMJ : British Medical Journal.

[45]  N. D. de Jong,et al.  Immune Evasion by Staphylococcus aureus , 2019, Microbiology spectrum.

[46]  G. Zhu,et al.  Organ- and host-specific clonal groups of Staphylococcus aureus from human infections and bovine mastitis revealed by the clumping factor A gene. , 2010, Foodborne pathogens and disease.

[47]  M. Mulvey,et al.  Regional Profiling for Determination of Genotype Diversity of Mastitis-Specific Staphylococcus aureus Lineage in Canada by Use of Clumping Factor A, Pulsed-Field Gel Electrophoresis, and spa Typing , 2009, Journal of Clinical Microbiology.

[48]  Henry F. Chambers,et al.  Waves of resistance: Staphylococcus aureus in the antibiotic era , 2009, Nature Reviews Microbiology.

[49]  K. Ko,et al.  Classification of Staphylococcal Cassette Chromosome mec (SCCmec): Guidelines for Reporting Novel SCCmec Elements , 2009, Antimicrobial Agents and Chemotherapy.

[50]  F. Lowy Staphylococcus aureus infections. , 2009, The New England journal of medicine.

[51]  P. François,et al.  Effect of a glucose impulse on the CcpA regulon in Staphylococcus aureus , 2009, BMC Microbiology.

[52]  F. DeLeo,et al.  Evolution of virulence in epidemic community-associated methicillin-resistant Staphylococcus aureus , 2009, Proceedings of the National Academy of Sciences.

[53]  E. Stobberingh,et al.  The evolution of Staphylococcus aureus. , 2008, Infection, genetics and evolution : journal of molecular epidemiology and evolutionary genetics in infectious diseases.

[54]  O. Schneewind,et al.  Panton-Valentine leukocidin is not a virulence determinant in murine models of community-associated methicillin-resistant Staphylococcus aureus disease. , 2008, The Journal of infectious diseases.

[55]  M. Ishii,et al.  Pediatric Pneumonia Death Caused by Community-acquired Methicillin-Resistant Staphylococcus aureus, Japan , 2008, Emerging infectious diseases.

[56]  Li Basuino,et al.  The arginine catabolic mobile element and staphylococcal chromosomal cassette mec linkage: convergence of virulence and resistance in the USA300 clone of methicillin-resistant Staphylococcus aureus. , 2008, The Journal of infectious diseases.

[57]  E. Feil,et al.  S. aureus IgG-binding proteins SpA and Sbi: host specificity and mechanisms of immune complex formation. , 2008, Molecular immunology.

[58]  E. Josefsson,et al.  In vivo sortase A and clumping factor A mRNA expression during Staphylococcus aureus infection. , 2008, Microbial pathogenesis.

[59]  G. Pugliese,et al.  Severe Streptococcus pyogenes Infections, United Kingdom, 2003–2004 , 2008, Emerging infectious diseases.

[60]  Timothy Foster,et al.  Key Role for Clumping Factor B in Staphylococcus aureus Nasal Colonization of Humans , 2008, PLoS medicine.

[61]  Atlanta,et al.  Invasive Methicillin-Resistant Staphylococcus aureus Infections in the United States , 2007 .

[62]  E. Greenberg,et al.  Generation of Virulence Factor Variants in Staphylococcus aureus Biofilms , 2007, Journal of bacteriology.

[63]  D. Coleman,et al.  The Emergence and Importation of Diverse Genotypes of Methicillin-Resistant Staphylococcus aureus (MRSA) Harboring the Panton-Valentine Leukocidin Gene (pvl) Reveal that pvl Is a Poor Marker for Community-Acquired MRSA Strains in Ireland , 2007, Journal of Clinical Microbiology.

[64]  J. Boyce,et al.  Emergence and resurgence of meticillin-resistant Staphylococcus aureus as a public-health threat , 2006, The Lancet.

[65]  P. Francioli,et al.  Evidence for Clonal Evolution among Highly Polymorphic Genes in Methicillin-Resistant Staphylococcus aureus , 2006, Journal of bacteriology.

[66]  Alex van Belkum,et al.  The role of nasal carriage in Staphylococcus aureus infections. , 2005, The Lancet. Infectious diseases.

[67]  Fran Lewitter,et al.  Intragenic tandem repeats generate functional variability , 2005, Nature Genetics.

[68]  A. van Belkum,et al.  Host- and Tissue-Specific Pathogenic Traits of Staphylococcus aureus , 2005, Journal of bacteriology.

[69]  Bruno Hoen,et al.  Staphylococcus aureus endocarditis: a consequence of medical progress. , 2005, Journal of the American Medical Association (JAMA).

[70]  S. Solomon,et al.  Methicillin-resistant–Staphylococcus aureus Hospitalizations, United States , 2005, Emerging infectious diseases.

[71]  William R Bishai,et al.  Community-acquired meticillin-resistant Staphylococcus aureus: an emerging threat. , 2005, The Lancet. Infectious diseases.

[72]  Susan K. Johnson,et al.  Comparison of community- and health care-associated methicillin-resistant Staphylococcus aureus infection. , 2003, JAMA.

[73]  D. Robinson,et al.  Evolutionary Models of the Emergence of Methicillin-Resistant Staphylococcus aureus , 2003, Antimicrobial Agents and Chemotherapy.

[74]  F. Vandenesch,et al.  Community-Acquired Methicillin-Resistant Staphylococcus aureus Carrying Panton-Valentine Leukocidin Genes: Worldwide Emergence , 2003, Emerging infectious diseases.

[75]  B. Spratt,et al.  How Clonal Is Staphylococcus aureus? , 2003, Journal of bacteriology.

[76]  Xiao Xue Ma,et al.  Insights on antibiotic resistance of Staphylococcus aureus from its whole genome: genomic island SCC. , 2003, Drug resistance updates : reviews and commentaries in antimicrobial and anticancer chemotherapy.

[77]  C. Walsh,et al.  The evolutionary history of methicillin-resistant Staphylococcus aureus (MRSA) , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[78]  B. Levin,et al.  Minimizing potential resistance: a population dynamics view. , 2001, Clinical infectious diseases : an official publication of the Infectious Diseases Society of America.

[79]  D. Livermore,et al.  Antibiotic resistance in staphylococci. , 2000, International journal of antimicrobial agents.

[80]  J. Hamilton-miller,et al.  Methicillin-resistant Staphylococcus aureus. , 1989, The New England journal of medicine.

[81]  R. Knox,et al.  “Celbenin” - resistant Staphylococci , 1961 .

[82]  J. Griffiths,et al.  Nasal Staphylococci and Sepsis in Hospital Patients , 1959, British medical journal.

[83]  W. M. Kirby EXTRACTION OF A HIGHLY POTENT PENICILLIN INACTIVATOR FROM PENICILLIN RESISTANT STAPHYLOCOCCI , 1944, Science.

[84]  A. Ogston Report upon Micro-Organisms in Surgical Diseases , 1881, British medical journal.

[85]  F. Lowy,et al.  Evolution of community- and healthcare-associated methicillin-resistant Staphylococcus aureus. , 2014, Infection, genetics and evolution : journal of molecular epidemiology and evolutionary genetics in infectious diseases.

[86]  G. Zhu,et al.  Repeat-based subtyping and grouping of Staphylococcus aureus from human infections and bovine mastitis using the R-domain of the clumping factor A gene. , 2009, Diagnostic microbiology and infectious disease.

[87]  H. Boucher,et al.  Epidemiology of methicillin-resistant Staphylococcus aureus. , 2008, Clinical infectious diseases : an official publication of the Infectious Diseases Society of America.

[88]  F. Tenover,et al.  The Epidemiology of Staphylococcus Infections , 2006 .

[89]  M. Ferraro Performance standards for antimicrobial susceptibility testing , 2001 .