Skip to main content

Methicillin resistant Staphylococcus Aureus in emergency department patients in the United Arab Emirates

Abstract

Background

Since the 1990s, community-associated methicillin resistant staphylococcus aureus (CA-MRSA) has emerged as an important global cause of skin and soft tissue infections. Little is known about the epidemiology of this pathogen in the Middle East.

Methods

We conducted a prospective observational study in a single large teaching hospital in Dubai to identify the incidence of community-acquired methicillin resistant staphylococcus aureus (MRSA) among ambulatory patients presenting with purulent skin and soft tissue infections. We performed wound cultures and administered standard questionnaires to 100 cases presenting to the emergency department. Bivariate and multivariate analyses were performed to identify risk factors for MSRA versus other pathogens.

Results

The prevalence of MRSA was 23% (18/78) among 78 culture-positive isolates and 29% (18/62) among Staphylococcus-positive isolates. 74% received antibiotics of which 4/74 (5%) received antibiotics appropriate for CA-MRSA infections. Multivariate adjusted analysis identified playing contact sports (OR 5.9 [95% CI 1.3–27.1]) and female sex (OR 6.3 [95% CI 1.6–24.8]) as independent risks for MRSA infection.

Conclusions

This is the first study to describe the epidemiology of CA-MRSA in the ambulatory setting in the Middle East and demonstrates a substantial proportion of cases presenting with skin and soft tissue infections were CA-MRSA. Although most skin and soft tissue infections are abscesses for which the cornerstone of treatment is high quality incision and drainage, if adjunct antibiotics are prescribed in this setting, CA-MRSA-active antibiotics should be considered.

Peer Review reports

Background

During the 1990s community-acquired MRSA (CA-MRSA) emerged in populations without exposure to health facilities and without traditional risk factors for MRSA [1, 2]. CA-MRSA infections exhibit different epidemiological characteristics, are resistant to fewer antibiotics, and express different toxin producing genes including, notably, the Panton-Valentine leucocidin a bicomponent toxin associated with recurrent skin and soft tissues infections (SSTIs) and necrotizing pneumonia [3].

CA-MRSA has emerged as a major global cause of purulent skin and soft tissues infections but little is known about the epidemiology of CA-MRSA in the Middle East [3,4,5] and no studies in the region have examined the prevalence of CA-MRSA in ambulatory settings. Given the absence of epidemiological data on this emerging pathogen we performed a cross-sectional observational study examining the prevalence of MRSA in purulent SSTI in ED patients in the United Arab Emirates (UAE). A secondary objective was to identify risk factors and clinical features of MRSA.

Methods

From January 2011, we prospective enrolled a convenience sample of 100 adult patients presenting with purulent SSTIs to the emergency department (ED) of Rashid Hospital and Trauma Centre, a 599-bed public, tertiary-care, urban teaching hospital in Dubai that serves a largely poor migrant worker population. The annual ED census is ~ 140,000. Approximately 85–90% of the Dubai population are expatriates with the majority originating from the Indian subcontinent.

Prior to study enrollment, standardized study protocol training was conducted for ED physicians and nurses including enrollment criteria, questionnaire administration, and culture swab collection. After obtaining consent, enrolling clinicians collected standardized information on epidemiological and clinical features, potential risk factors, treatment and disposition (Table 1). Exclusion criteria included patients below the age of 18 years, hospitalization within the previous week, Bartholin, odontogenic or perianal abscesses, and infected post-operative incisional sites. We defined community-acquired MRSA according to United States Centers for Disease Control and Prevention criteria: (1) Positive culture for MRSA as an outpatient or within 48 h of hospital admission; (2) No medical devices or indwelling catheters that are permanently placed though the skin; (3) No history of MRSA infections; and (4) No recent history of hospitalization or residence in nursing home or long-term care facility. [6] Antibiotic sensitivity testing was performed using standard MIC and disk diffusion RH sensitivity methods.

Table 1 Univariate risk factors for MRSA infection versus other bacterial pathogens among emergency department patients with purulent skin and soft tissue infections

Crude and adjusted analyses using logistical regression to identify variables associated with MRSA versus other bacterial isolates were performed using IBM SPSS (V 19). A multivariate model using backward stepwise elimination was performed using all risk variables. Significance assumes p < 0.05 or an Odds Ratio (OR) that does not cross one.

Ethics approval and consent to participate

All study participants provided written informed consent to participate in this study. The Medical Research Committee of the Dubai Health Authority, UAE, approved this study (October 2010).

Results

Between January 2011 and June 2012, 99 patients with purulent SSTI infections were enrolled in the study and provided 100 culture samples (one patient with recurrent SSTI provided two specimen cultures 6 weeks apart); 75 (75%) were male with a median age of 30 (range 16–64); 74 (74%) were expatriates and 26% Emirati nationals. A bacterial culture isolate was identified in 78 patients including 44 methicillin-sensitive Staphylococcus aureus (SSSA) isolates and 18 MRSA isolates; other organisms were isolated from 16 patients. No organism was identified in 22 patients. When considering all patients enrolled, MRSA was isolated in 18 of 100 cases (18%); when considering only positive isolates, 18 of 78 (23%) were MRSA-positive. Of 62 total S. aureus isolates, 18 (29%) were MRSA positive. Seventeen of 18 MRSA cases (94%) met the criteria for CA-MRSA (one case had been hospitalized < 3-months prior to enrollment). Potential risk factors stratified by MRSA versus other bacteria isolates are listed in Table 1.

Multivariate adjusted analysis identified female sex (OR 6.3 [95% CI 1.6–24.8]) and playing contact sports (OR 5.9 [95% CI 1.3–27.1]) as independent risks for MRSA infection. A total of 74 patients (74%) received antibiotics of which 4/74 (5%) were antibiotics routinely recommended for CA-MRSA infections including clindamycin (3) and doxycycline (1). All of the 18 MRSA isolates were susceptible to trimethoprim-sulfamethoxazole in addition to vancomycin and linezolid. Isolates were not routinely tested for clindamycin or erythromycin susceptibility. There was no difference in the proportion of MRSA-positive cases versus non-MRSA positive cases requiring hospitalization (11/18, 61% versus 36/60, 60%, p = 0.33).

Discussion

We present the first study in the Middle East to describe the epidemiological features of CA-MRSA among ambulatory patients presenting with SSTI. The overall prevalence of MRSA was 18% and the prevalence of MRSA among S. aureus isolates was 29%. The CA-MRSA prevalence reported in this study, although not as high as the United States, [7, 8] are similar to those recently reported in a multi-centre European study in which an average of 15% of SSTIs presenting to EDs were CA-MRSA, although substantial geographic variability was reported [9]. A number of studies have examined molecular characteristics of CA-MRSA in the UAE and Middle East or the prevalence of MRSA among laboratory S. aureus isolates [10,11,12,13,14,15,16] but no regional study has described the prevalence and epidemiology of MRSA among ambulatory patients.

Our study identified female sex and playing contact sports as independent risk factors for MRSA infection. Although playing contact sports is a well described risk factors for CA-MRSA in other settings, the association of female sex with MRSA was unexpected and requires further study. The risk of CA-MRSA versus other bacterial isolate was not different between the local Emirate and expatriate populations. Other risk factors were not identified, perhaps due to the relatively small sample size of this study or due to widespread community transmission of CA-MRSA beyond narrow epidemiological niches, which makes the identification of specific risk factors more challenging. Clinicians were not able to discriminate between MRSA and non-MRSA infections in this study.

Although most SSTI cases were treated with antibiotics, only a small proportion were treated with CA-MRSA-active antibiotics, a finding that is consistent with anecdotal observations that awareness of CA-MRSA as an important cause of purulent SSTI among healthcare providers is low. A substantial and likely increasing proportion of patients in this setting are likely to be infected with MRSA that will not respond to treatment with beta-lactam antibiotics including cephalosporins and combination or newer generation penicillins (for example amoxicillin-clavulanic acid). If antibiotic treatment is being considered as primary or adjunct treatment for purulent SSTI due to CA-MRSA, the Infectious Disease Society of American (IDSA) recommend clindamycin, trimethoprim-sulfamethoxazole, tetracyclines (minocycline, doxycycline) or Linazolid.

Historically, the management of purulent SSTI, particularly abscesses, has been incision and drainage, regardless of whether or not the responsible organism is MRSA. Recent data from the US, however, indicates that treatment with trimethoprim-sulfamethoxazole, which is active against most CA-MRSA strains, in addition to incision and drainage, improves cure rates in ED patients [7]. In that study, however, MRSA prevalence rates were ~ 45% raising questions about whether trimethoprim-sulfamethoxazole should be prescribed to patients with purulent SSTIs in countries where CA-MRSA prevalence rates may be lower. Regardless, if antibiotics are being considered in addition to standard incision and drainage, clinicians should be aware that in this setting one in four patients presenting to an ED with a purulent SSTI may be infected with CA-MRSA.

Limitations of this study include the small sample size and the longer-than expected enrollment period suggesting cases may have been missed and potentially risking selection bias. No molecular typing of samples was performed which would provide additional insight into the circulating strains and molecular epidemiology of CA-MRSA in the UAE.

Conclusion

Given the global CA-MRSA epidemic will continue to evolve and given the UAE and the Middle East region will likely experience increasing rates of CA-MRSA-related disease in the future, clinicians should be prepared for and comfortable with managing SSTIs and other related conditions.

Abbreviations

CA-MRSA:

Community-associated methicillin-resistant staphylococcus aureus

ED:

Emergency department

IDSA:

Infectious Disease Society of American

SSTI:

Skin and soft tissue infection

References

  1. Barrett FF, McGehee RF, Finland M. Methicillin-resistant Staphylococcus aureus at Boston City Hospital. N Engl J Med. 1968;279(9):441–8.

    Article  PubMed  CAS  Google Scholar 

  2. Herold BC, Immergluck LC, Maranan MC, Lauderdale DS, Gaskin RE, Boyle-Vavra S, et al. Community-acquired methicillin-resistant Staphylococcus aureus in children with no identified predisposing risk. JAMA. 1998;279(8):593–8.

    Article  PubMed  CAS  Google Scholar 

  3. Zetola N, Francis JS, Nuermberger EL, Bishai WR. Community-acquired meticillin-resistant Staphylococcus aureus: an emerging threat. Lancet Infect Dis. 2005;5(5):275–86.

    Article  PubMed  Google Scholar 

  4. Pallin DJ, Egan DJ, Pelletier AJ, Espinola JA, Hooper DC, Camargo CA. Increased US emergency department visits for skin and soft tissue infections, and changes in antibiotic choices, during the emergence of community-associated methicillin-resistant Staphylococcus aureus. Ann Emerg Med. 2008;51(3):291–8.

    Article  PubMed  Google Scholar 

  5. Qualls ML, Mooney MM, Camargo CA, Zucconi T, Hooper DC, Pallin DJ. Emergency department visit rates for abscess versus other skin infections during the emergence of community-associated methicillin-resistant Staphylococcus aureus, 1997-2007. Clin Infect Dis. 2012;55(1):103–5.

    Article  PubMed  Google Scholar 

  6. Maree CL, Daum RS, Boyle-Vavra S, Matayoshi K, Miller LG. Community-associated methicillin-resistant Staphylococcus aureus isolates and healthcare-associated Infections1. Emerg Infect Dis. 2007;13(2):236–42.

    Article  PubMed  PubMed Central  Google Scholar 

  7. Talan DA, Mower WR, Krishnadasan A, Abrahamian FM, Lovecchio F, Karras DJ, et al. Trimethoprim–sulfamethoxazole versus placebo for uncomplicated skin abscess. N Engl J Med. 2016;374(9):823–32.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  8. Moran GJ, Krishnadasan A, Gorwitz RJ, Fosheim GE, McDougal LK, Carey RB, et al. Methicillin-resistant Staphylococcus aureus infections among patients in the emergency department. N Engl J Med. 2006;355(7):666–74.

  9. Bouchiat C, Curtis S, Spiliopoulou I, Bes M, Cocuzza C, Codita I, et al. MRSA infections among patients in the emergency department: a European multicentre study. J Antimicrob Chemother. 2017;72(2):372–75.

  10. Aly M, Balkhy HH. The prevalence of antimicrobial resistance in clinical isolates from gulf corporation council countries. Antimicrob Resist Infect Control. 2012;1:26.

    Article  PubMed  PubMed Central  Google Scholar 

  11. Udo EE, Al-Sweih N, Dhar R, Dimitrov TS, Mokaddas EM, Johny M, et al. Surveillance of antibacterial resistance in Staphylococcus aureus isolated in Kuwaiti hospitals. Med Princ Pract. 2008;17:71–5.

  12. Dash N, Panigrahi D, Al Zarouni M, Yassin F, Al-Shamsi M. Incidence of community-acquired methicillin-resistant Staphylococcus aureus carrying pantone-valentine leucocidin gene at a referral hospital in United Arab Emirates. APMIS. 2014;122(4):341–6.

    Article  PubMed  CAS  Google Scholar 

  13. Sonnevend Á, Blair I, Alkaabi M, Jumaa P, al Haj M, Ghazawi A, et al. Change in methicillin-resistant Staphylococcus aureus clones at a tertiary care hospital in the United Arab Emirates over a 5-year period. J Clin Pathol. 2012;65(2):178–82.

    Article  PubMed  Google Scholar 

  14. 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(1):146.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  15. Senok A, Somily A, Raji A, Gawlik D, Al-Shahrani F, Baqi S, et al. Diversity of methicillin-resistant Staphylococcus aureus CC22-MRSA-IV from Saudi Arabia and the Gulf region. Int J Infect Dis. 2016;51:31–5.

    Article  PubMed  CAS  Google Scholar 

  16. Udo EE, Al-Lawati BA-H, Al-Muharmi Z, Thukral SS. Genotyping of methicillin-resistant Staphylococcus aureus in the Sultan Qaboos University Hospital, Oman reveals the dominance of Panton–valentine leucocidin-negative ST6-IV/t304 clone. New Microbes New Infect. 2014;2(4):100–5.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

Download references

Availability of data and materials

The datasets used and/or analysed during the current study are available from the corresponding author on reasonable request.

Author information

Authors and Affiliations

Authors

Contributions

MAJ and HF participated in the design of the study, study coordination, data collection, data analysis, and drafting the manuscript. RA participated in data collection and drafting the manuscript. FN participated in the design of the study, study coordination, and drafting the manuscript. ZAD and RS provided laboratory support and participated in study design. EN conceived the study and participated in the design, study coordination, data analysis, and drafting the manuscript. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Eric J. Nilles.

Ethics declarations

Ethics approval and consent to participate

All study participants provided written informed consent to participate in this study. The Medical Research Committee of the Dubai Health Authority, UAE, approved this study (October 2010).

Competing interests

The authors declare that they have no competing interests.

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Al Jalaf, M., Fadali, H., Alanee, R. et al. Methicillin resistant Staphylococcus Aureus in emergency department patients in the United Arab Emirates. BMC Emerg Med 18, 12 (2018). https://doi.org/10.1186/s12873-018-0164-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1186/s12873-018-0164-7

Keywords