Skip to content

Advertisement

  • Research note
  • Open Access

Nasal carriage, risk factors and antimicrobial susceptibility pattern of methicillin resistant Staphylococcus aureus among healthcare workers in Adigrat and Wukro hospitals, Tigray, Northern Ethiopia

  • 1, 2Email author,
  • 1,
  • 1,
  • 1,
  • 1, 2,
  • 1 and
  • 1
BMC Research Notes201811:250

https://doi.org/10.1186/s13104-018-3353-2

  • Received: 5 February 2018
  • Accepted: 11 April 2018
  • Published:

Abstract

Objective

The aim of this study was to determine nasal carriage, risk factors and antimicrobial susceptibility pattern of methicillin resistant Staphylococcus aureus among health care-workers of Adigrat and Wukro hospitals Northern Ethiopia.

Results

The overall prevalence of S. aureus and methicillin resistance S. aureus (MRSA) in the present study were 12% (29/242) and 5.8% (14/242) respectively. The rate of MRSA among S. aureus was 48.3%(14/29). In this study, MRSA carriage was particularly higher among nurse professionals (7.8%) and surgical ward (17.1%). None of the MRSA isolates were sensitive to penicillin and ampicillin. However, low resistance was found for chloramphenicol and clindamycin. Being diabetic and use of hands rub was statistically significant with MRSA colonization.

Keywords

  • Antimicrobial susceptibility test
  • Health care workers
  • methicillin resistance Staphylococcus aureus
  • nasal carriage
  • Staphylococcus aureus

Introduction

Staphylococcus aureus is known to be the cause of hospital and community acquired infections [1]. Methicillin resistant S. aureus (MRSA) causes a significant problem of the world and major health care associated pathogen [2, 3]. About 10–35% world population harbors MRSA in their anterior nares [4]. The emergence of MRSA is an important hospital acquired pathogen continues to remain a significant factor for failure of patient management worldwide [35].

Increasing rates of antibiotic resistance owing to an incautious use of antimicrobials lead to decrease treatment options for MRSA infection [6]. The increasing of MRSA strains becomes a public health problem [3]. This has a negative effect on the treatment cost, long hospitalization, and increased morbidity and mortality especially among the critically ill patients [7]. The problem of MRSA is observed all over the world, although, the burden of infection is high in developing countries [8].

High MRSA carriages of health care professionals have been reported as the key mechanism of transmission among patients during treatments, patients contact and aerosolization following sneezing [9]. Health care workers who have direct contact between the community and hospital may serve as the agents of the cross-transmission of the community acquired and hospital acquired MRSA [10].

Knowledge of MRSA prevalence and recent antimicrobial susceptibility pattern is very important for appropriate selection of the antimicrobial agents [11]. However, in most hospitals of African countries, there is neither surveillance system nor control policy for MRSA, this plays significant role for increasing the problem [12].

Therefore, this current study was aimed to determine nasal carriage, antimicrobial susceptibility patterns and associated factors of MRSA colonization among healthcare workers in Adigrat and Wukro hospitals, Tigray, northern Ethiopia. This evidence based information in the study area will contribute a role for the prevention and control of MRSA by responsible bodies.

Main text

Methods

Study area and study design

This study was carried out in Wukro and Adigrat general hospitals. Those hospitals are found in eastern zone of Tigray region and are located about 824 and 900 km respectively north of Addis Ababa (Capital city of Ethiopia). Wukro and Adigrat general hospitals have a total staffs 313 among those 41.3% are males and 58.7% are female, and are serve for the total population of 755,343. A cross sectional study was carried out among 242 health care workers from September to December 2016.

Isolation and identification

Swabs were inoculated on Manitol Salt agar (MSA) (Oxid, UK) and incubated at 37 °C for 24 h and sub cultured into blood agar. All positive culture was identified by their characteristics appearance and biochemical test using standard procedure. Colonies that were Manitol fermented (golden yellow colonies), β-hemolytic on blood agar were considered as S. aureus and was confirmed by Coagulase test as positive [13].

Antimicrobial susceptibility testing

Antimicrobial susceptibility testing was performed using modified Kirby–Bauer disc diffusion method on Muller–Hinton agar (MHA; Oxoid, UK) according Clinical and Laboratory Standards Institute (CLSI, 2016) guidelines [14]. From overnight grown colonies on nutrient agar 3–5 well-isolated colonies were emulsified in 3–4 ml of sterile physiological saline to get bacterial inoculums equivalent to 0.5 McFarland turbidity standards. After that the antibiotic discs were placed manually on the medium and incubated at 37 °C for about 18 h and the zones of inhibition was measured using caliper. The interpretation of the results was made based on the CLSI criteria as sensitive, intermediate and resistant [14]. Cefoxitin discs (30 μg), penicillin (10 μg), ampicillin (10 µg), erythromycin (15 µg), cotrimoxazol (25 µg), chloramphenicol (30 µg), gentamycin (10 µg), kanamycin (30 µg), amikacin (30 µg), ciprofloxacin (5 µg), tetracycline (30 µg), and clindamycin (2 µg) (Oxoid, UK). All isolates resistant to cefoxitin was considered as MRSA [14].

Data processing and analysis

The findings were statically analyzed using descriptive statistics, Chi square test (χ2) and p < 0.05 was considered as statistically significant. The variables from the demographic and associated risk analysis were performed using SPSS (version 22) package.

Results

Socio-demographic characteristics

A total of 242 health professionals were included in the study. The age of study participants ranged from 20 to 59 years with mean age of 31.78 ± 8.9 years. One hundred forty-two (58.7%) were females and 100 (41.3%) were males. The mean number of their work experience was 9.1 years.

Prevalence of Staphylococcus aureus and MRSA

The prevalence of S. aureus and MRSA in this study was 12% (29/242) and 5.8% (14/242) respectively. The prevalence of MRSA among nurse, doctor and midwife professionals were 10 (7.8%), 1 (7.7%), and 2 (6.7%) respectively. The highest rate of S. aureus and MRSA observed in surgical ward were 7 (20.0%) and 6 (17.1%) respectively (Additional file 1: Table S1).

Risk factors associated for MRSA colonization

Chi square test (χ2) showed that use of hand rub (p < 0.001), and being a diabetic (p < 0.001), were statistically significant with MRSA colonization (Table 1).
Table 1

Risk factors associated with MRSA colonization among health professionals at Adigrat and Wukro hospitals, Tigray, Northern Ethiopia September–December 2016

Variable

MRSA

p value

No, n (%)

Yes, n (%)

Sex

 Male

93 (93)

7 (7.0)

0.497

 Female

135 (95.1)

7 (4.9)

 

Age group

 20–29

129 (94.2)

8 (5.8)

0.503

 30–39

52 (91.2)

5 (8.8)

 

 40–49

30 (96.8)

1 (3.2)

 

 50–59

17 (100)

0 (0.0)

 

Work experience

 < 5

110 (94)

7 (6.0)

0.486

 6–10

56 (96.6)

2 (3.4)

 

 11–20

22 (88)

3 (12.0)

 

 21–30

40 (95.2)

2 (4.8)

 

Department

 Medical

26 (96.3)

1 (3.7)

0.081

 Surgical

29 (82.9)

6 (17.1)

 

Pediatric

20 (90.9)

2 (9.1)

 

 Gynecology and obstetrics

28 (93.3)

2 (6.7)

 

 Laboratory

25 (100)

0 (0.0)

 

 Outpatient department

48 (96)

2 (4.0)

 

 Pharmacy

25 (96.2)

1 (3.8)

 

 Others

27 (100)

0 (0.0)

 

Hand washing habit

 Always

116 (94.3)

7 (5.7)

0.298

 Usually

91 (95.8)

4 (4.2)

 

 Rare

21 (87.5)

3 (12.5)

 

Use of hand rub

 Always

123 (99.2)

1 (0.8)

0.001*

 Usually

97 (95.1)

5 (4.9)

 

 Rare

8 (50)

8 (50)

 

Prior hospitalization

 Yes

23 (88.5)

3 (11.5)

0.183

 No

205 (94.9)

11 (5.1)

 

History of antibiotics treatment

 Yes

115 (92)

10 (8)

0.127

 No

113 (96.6)

4 (3.4)

 

Chronic obstructive pulmonary disease

 Yes

28 (87.5)

4 (12.5)

0.081

 No

200 (95.2)

10 (4.8)

 

Diabetic mellitus

 Yes

7 (70)

3 (30.0)

0.001*

 No

221 (95.3)

11 (4.7)

 

*Statistically significant with MRSA colonization

NB: use of hand rub is use of a waterless alcohol [30]

Antimicrobial susceptibility patterns of Staphylococcus aureus

The antimicrobial Susceptibility patterns were performed for the 29 S. aureus isolates against 12 antimicrobials. Of the 29 isolates, 93.1% showed resistance to penicillin followed by kanamycin 19 (65.5%), erythromycin 18 (62.1%), tetracycline 16 (55.2%) cotrimoxazole 15 (51.7%), ampicillin 14 (48.3%), and amikacin 13 (44.8%). Low resistance were found for chloramphenicol 5 (17.2%) and clindamycin 5 (17.2%). None of the isolates were intermediate resistance (Fig. 1).
Fig. 1
Fig. 1

Antimicrobial susceptibility pattern of S. aureus strains to different antimicrobial agents at Adigrat and Wukro hospitals, Tigray, Northern Ethiopia September–December 2016 (n = 29)

Antimicrobial susceptibility pattern of methicillin resistance S. aureus (Additional file 2: Figure S1, Additional file 3: Table S2)

Multidrug resistance of Staphylococcus aureus isolates
According to Magiorakos et al. [15], multi-drug resistance in this study was considered as resistance to three or more of the antimicrobial class tested. Twenty-two (75.9%) of all the isolates were multi-drug resistant, five isolates were resistant for three and two isolates were resistant for ten antimicrobials (Table 2).
Table 2

Multi-drug resistance nature of S. aureus isolates at Adigrat and Wukro hospitals, Tigray, Northern Ethiopia September–December 2016

 

Antibiotics

Number (%)

For three

PEN, AMP, CXT

2 (9.2%)

PEN, ERY, TTC

1 (4.54%)

PEN, ERY, AK

1 (4.54%)

PEN, TTC, AK

1 (4.54%)

For four

PEN, ERY, TTC, AK

1 (4.54%)

PEN, AMP, TTC, CXT

1 (4.54%)

PEN, AMP, TTC, CXT

1 (4.54%)

For six

PEN, DA, TS, CIP, TTC, AK

1 (4.54%)

PEN, GM, TS, CIP, TTC, AK

1 (4.54%)

PEN, AMP, TS, TTC, AK, CXT

1 (4.54%)

For seven

PEN, DA, ERY, GM, TS, CIP, CHL

1 (4.54%)

PEN, AMP, ERY, GM, TS, CIP, CXT

1 (4.54%)

For eight

PEN, ERY, GM, TS, CIP, CHL, TTC, AK

1 (4.54%)

PEN, AMP, ERY, GM, TS, CIP, TTC, CXT

1 (4.54%)

PEN, AMP, ERY, GM, TS, CHL, AK, CXT

1 (4.54%)

PEN, AMP, DA, ERY, CIP, TTC, AK, CXT

1 (4.54%)

PEN, AMP, ERY, GM, TS, CIP, TTC, CXT

1 (4.54%)

PEN, AMP, ERY, GM, TS, TTC, AK, CXT

1 (4.54%)

PEN, AMP, ERY, GM, TS, CIP, AK, CXT

1 (4.54%)

For ten

PEN, AMP, DA, ERY, GM, TS, CHL, TTC, AK, CXT

1 (4.54%)

PEN, AMP, DA, ERY, GM, TS, CIP, CHL, TTC, CXT

1 (4.54%)

Total

22 (100%)

PEN penicillin, AMP ampicillin, GM gentamycin, AK amikacin, CHL chloramphenicol, CIP ciprofloxacin, TTC tetracycline, TS cotrimoxazol, DA clindamycin, ERY erythromycin, K kanamycin, CXT cefoxitin

MDR multidrug resistant; MDR definition for S. aureus percent is computed from total number of S. aureus

Discussion

The overall nasal carriage of S. aureus in the present study was 12%. This is supported by study carried out in India (14%) [10]. However, lower than that of reported from Ethiopia, (28.8%) [13], Democratic Republic Congo (16.5%) [16], Gaza Strip (31.1%) [17] Pakistan (48%) [18], China (25.3%) [19] and Iran (25.7%) [20].

The total prevalence of MRSA in this study was 5.78%. This was similar with results from [8], France (5.3%) [21], Asia (6.1%) [8] and Iran (5.3%) [20]. However, it was lower compared with the study revealed in Ethiopia, Mekelle (14.1%) [22] and Dessie (12.7%) [13], Egypt (20%) [23], Nigeria (39.9%) [12], Gaza Strip (25.5%) [17] and Pakistan (13.95%) [18]. On the other hand, our result was higher than study reported from and China (1.0%) [19]. This variations of prevalence among different study areas might be due to difference in rate of patient admission, study period [22], microbiological methods (from sample size to culture media) antimicrobial policy, in addition to that, variety levels of commitment to infection prevention measure among hospitals, and awareness of the health care worker about MRSA may contribute to the difference.

In current study, MRSA carriage was relatively higher among nurses (7.8%) followed by doctors (7.7%). This is consistent with study conducted in Ethiopia, Dessie [13], Gaza Strip [17] and India [10]. MRSA carriage was particularly high among surgical ward (17.1%) this result is comparable with corresponding study in Gaza Strip (35%) [17] and Dessie (35%) [13]. This result might be explained by the frequent direct physical contact of doctors and nurses with patients and increase workload in surgical wards.

In this study, use of hands was statistically significant with MRSA colonization. Health care workers rarely used hand rub were high proportion to have MRSA colonization on their anterior nare than those who were used hand rub usually and always. This finding is in line to previous studies in America [7], France [21], and Taiwan [24]. The temporary hand carriage of bacteria on the hands of health professionals could account for the major mechanism for the auto-transmission from contaminated hand to nose.

The present study, found that being diabetic patients was statistically associated with MRSA colonization. Health care workers with diabetic were high proportion to have MRSA colonization on their anterior nare. This was in line with studies from Tanzania [25] Iran [20], and Taiwan [26]. This may be due to diabetic patients reduced immunity which fails to combat the pathogens [25].

In the current study, there was no statistically significant of MRSA with educational status, hand washing habit, prior hospitalization, history of antibiotic treatment, and presence of chronic obstructive pulmonary disease in this study. This was in agreement with a result obtained in Ethiopia [13] and other studies conducted in other parts of the world [8, 20, 27].

Concerning antimicrobial susceptibility patterns of MRSA isolates, clindamycin and chloramphenicol were effective against MRSA isolates. However, increasing resistance was observed in our finding which is consistent with study reported from Pakistan ampicillin, penicillin, erythromycin, amikacin and ciprofloxacin (100%), (100%), (66%), (44%), and (33%) respectively [18]. Cotrimoxazole also showed a similar result compared with corresponding reports of Dessie (66.7%) [11]. Despite slight differences in the reported figures, the susceptibility patterns of antimicrobial were in line with the study from Nigeria for gentamycin 50 (63.3%), erythromycin 55 (69.6%) and Ciprofloxacin 32 (40.5%) [12], in India [3] for ciprofloxacin (34.6%) and erythromycin (54.8%), chloramphenicol (16.1%) from Serbia [27], and penicillin (93%) reported from India [10].

Higher susceptibility was also showed in the present study as compared to a result from health care workers at Iran for gentamycin (69%), clindamycin (69%), and ciprofloxacin (66%) [20]. Kanamycin also showed lower resistance compared with similar study in Serbia (90.3%) [27]. On the other hand, our finding was higher compared to studies conducted in India [28] ciprofloxacin (20%), and Gaza Strip erythromycin, tetracycline, gentamycin, clindamycin, and ciprofloxacin (19.6%), (9.8%), (3.9%), (3.92%), and (3.92%) respectively [17]. This resistance pattern of our finding might be due to excessive use of this antibiotics for many other infections and replacing of sensitive strains by resistance strains at the hospital settings.

Drug susceptibility test on all the 29 S. aureus isolates against 12 commonly used antibiotics were performed. The resistance of strains against penicillin, ciprofloxacin, and erythromycin is consistent with studies conducted in Ethiopia, Dessie [11], and Nepal [6], but cotrimoxazole (81.7%) and gentamycin (60.4%) were higher than our finding. However, lower resistance was observed with cotrimoxazole (33%), and gentamycin (27%) conducted in India [10], and 25% for gentamycin in Nepal [29]. This might be due to the variation in the geographical area, and local infection prevention and control strategies of the hospital settings.

Studies conducted in Ethiopia and China has reported higher resistance patterns to tetracycline (71.4%), chloramphenicol (57.1%) [11] and clindamycin (70%) [19]. Where as lower resistance than our finding to amikacin was reported from India [10], Nepal [6], and Pakistan [18]. In the present study higher resistance were showed for tetracycline, cotrimoxazol and gentamycin compared with study conducted in India [10]. In our study area, penicillin, ampicillin and erythromycin are the commonly prescribed antibiotics. This might have contributed for the resistance against these antimicrobials.

In this study high prevalence of multi drug resistance to wards S. aureus was observed. Of the total isolates 22 (75.9%) were resistant to three and above class of antimicrobials [15]. Fourteen of them (63.6%) were MRSA and comparable susceptibility was observed in a study from Ethiopia, Dessie [11]. This increased multi drug resistance might be due to continuous genetic variation of strains by mutation, or cross transmission of the a resistance genetic elements from one to another bacterium, overcrowded wards, and prescribed of antibiotics without culture and sensitivity [18].

Conclusions

The present study, the overall prevalence of MRSA in the study area was found to be 5.78%. The carriage rate MRSA was worse among nurses and working in surgical wards. Rarely used hand rub and being diabetics were statistically significant with MRSA colonization. Clindamycin and chloramphenicol were sensitive antimicrobials for the treatment of MRSA and S. aureus. The majority of the S. aureus isolates were multidrug resistant.

Limitation of the study

The infection is due to community or hospital acquired strains could not be identified. More sensitive and specific molecular techniques could not be used to identify the species and strain typing of S. aureus.

Furthermore, for the future researcher phenotypic and genotypic studies are needed to establish and clarify the genetic mechanism behind susceptibilities to antibiotics.

Abbreviations

AST: 

antimicrobial susceptibility testing

CLSI: 

Clinical and Laboratory Standards Institute

MDR: 

multi-drug resistance

MRSA: 

methicillin resistant Staphylococcus aureus

MSSA: 

methicillin sensitive Staphylococcus aureus

Declarations

Authors’ contributions

HL designed the study, collection, analysis, and interpretation of data, and drafted the manuscript. AG, AGK, and AK designed the study, supervised data collection both on field and in laboratory, and prepared the manuscript. All authors read and approved the final manuscript.

Acknowledgements

The authors gratefully acknowledge the health care workers of study area for their participation on study. We also wish to extend our deep appreciation to Mekelle University, College of Health Sciences for providing us the opportunity to do this thesis writing, and allowing the laboratory space with material supports.

Competing interests

The authors declare that they have no competing interests.

Availability of data and materials

All data collected and analyzed during this study were included in the manuscript. But if the full paper is needed, it will be shared upon request by the editor from the corresponding author.

Consent for publication

Not applicable.

Ethics approval and consent to participate

The study was approved by College of health sciences Research ethical review committee of Mekelle University, Ethiopia (Consent Ref Number 0814/2016 approval dated 16/08/2016. Official letter was obtained from Tigray regional health bureau to Adigrat and Wukro hospitals (Consent Ref Number 01/1418/2016 approval dated 10/09/2016. Permission was also obtained from administrative of each hospital and other concerns. Written informed consent was sought from each study participants before sample collection and maintained throughout the study. All participants were given code numbers to keep their identity confidential.

Funding

Not applicable.

Publisher’s Note

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

Open AccessThis 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.

Authors’ Affiliations

(1)
Department of Microbiology and Immunology, Institute of Biomedical Sciences, College of Health Science, Mekelle University, Mekelle, Ethiopia
(2)
Department of Medical Laboratory, College of Medicine and Health Science, Adigrat University, Adigrat, Ethiopia

References

  1. Chen CS, Chen CY, Huang YC. Nasal carriage rate and molecular epidemiology of methicillin-resistant Staphylococcus aureus among medical students at a Taiwanese university. Int J Infect Dis. 2012;16:799–803.View ArticleGoogle Scholar
  2. Grundmann H, Aires-de-Sousa M, Boyce J, Tiemersma E. Emergence and resurgence of meticillin-resistant Staphylococcus aureus as a public-health threat. Lancet. 2006;368(9538):874–85.View ArticlePubMedGoogle Scholar
  3. Goyal A, Diwakar MK, Bhooshan S, Goyal S, Agrawal A. Prevalence, and antimicrobial susceptibility pattern of methicillin-resistant Staphylococcus aureus [MRSA] isolates at a tertiary care hospital in Agra, North India—a systemic annual review IOSR. J Dent Med Sci. 2013;11(6):80–4.Google Scholar
  4. Moniri R, Musav GA, Fadavi N. The prevalence of nasal carriage methicillin-resistant Staphylococcus aureus in hospitalized patients. Pak J Med Sci. 2009;25(4):656–9.Google Scholar
  5. Habeeb A, Hussein NR, Assafi MS, Al-Dabbagh SA. Methicillin resistant Staphylococcus aureus nasal colonization among secondary school students. J Microbiol Infect Dis. 2014;4(2):59–63.View ArticleGoogle Scholar
  6. Ansari S, Nepal HP, Gautam R, Rayamajhi N, Shrestha S, Upadhyay G, et al. Threat of drug resistant Staphylococcus aureus to health in Nepal. BMC Infect Dis. 2014;14(157):1–5.Google Scholar
  7. Chamchod F, Ruan S. Modeling the spread of methicillin-resistant Staphylococcus aureus in nursing homes for elderly. PLoS ONE. 2012;7(1):e29757.View ArticlePubMedPubMed CentralGoogle Scholar
  8. Morgenstern M, Erichsen C, Hackl S, Mily J, Militz M, Friederichs J, et al. Antibiotic resistance of commensal Staphylococcus aureus and coagulase-negative Staphylococci in an international cohort of surgeons: a prospective point-prevalence study. PLOS ONE. 2016;11(2):e0148437.View ArticlePubMedPubMed CentralGoogle Scholar
  9. Gurieva TV, Bootsma MC, Bonten MJ. Decolonization of patients and health care workers to control nosocomial spread of methicillin-resistant Staphylococcus aureus: a simulation study. BMC Infect Dis. 2012;12:302.View ArticlePubMedPubMed CentralGoogle Scholar
  10. Malini J, Harle SA, Padmavathy M, Umapathy BL, Navaneeth BV, Keerthi Mannan J, et al. Methicillin resistant Staphylococcus aureus carriage among the health care workers in a tertiary care hospital. J Clin Diagn Res. 2012;6(5):791–3.Google Scholar
  11. Shibabaw A, Abebe T, Tihret A. Antimicrobial susceptibility pattern of nasal Staphylococcus aureus among Dessie referral hospital health care workers, Dessie, Northeast Ethiopia. Int J Infect Dis. 2014;25:22–5.View ArticlePubMedGoogle Scholar
  12. Fadeyi A, Bolaji BO, Oyedepo OO, Adesiyun OO, Adeboye MAN, Olanrewaju TO, et al. Methicillin resistant Staphylococcus aureus carriage amongst healthcare workers of the critical care units in a Nigerian hospital. Am J Infect Dis. 2010;6(1):18–23.View ArticleGoogle Scholar
  13. Shibabaw A, Abebe T, Tihret A. Nasal carriage rate of methicillin resistant Staphylococcus aureus among Dessie referral hospital health care workers; Dessie, Northeast Ethiopia. Antimicrob Resist Infect Control. 2013;2(25):1–5.Google Scholar
  14. Clinical and Laboratory standards Institute (CLSI). Performance standards for antimicrobial susceptibility testing; Twenty-sixth Informational Supplement. Wayne PA 19087 USA 2016; 36(1).Google Scholar
  15. Magiorakos AP, Srinivasan A, Carey RB, Carmeli Y, Falagas ME, Giske CG, et al. Multidrug-resistant, extensively drug-resistant, and pandrug-resistantbacteria: an international expert proposal for interim standard definitions for acquired resistance. Clin Microbiol Infect. 2012;18:268–81.View ArticlePubMedGoogle Scholar
  16. De Boeck H, Vandendriessche S, Hallin M, Batoko B, Alworonga JP, Mapendo B, et al. Staphylococcus aureus nasal carriage among healthcare workers in Kisangani, the Democratic Republic of the Congo. Eur J Clin Microbiol Infect Dis. 2015;34:1567–72.View ArticlePubMedGoogle Scholar
  17. El Aila NA, Al Laham NA, Ayesh BM. Nasal carriage of methicillin resistant Staphylococcus aureus among health care workers at Al Shifa hospital in Gaza Strip. BMC Infect Dis. 2017;17(28):1–7.Google Scholar
  18. Rashid Z, Farzana K, Sattar A, Murtaza G. Prevalence of nasal Staphylococcus aureus and methicillin-resistant Staphylococcus aureus in hospital personnel and associated risk factors. Acta Pol Pharm. 2012;69(5):985–91.PubMedGoogle Scholar
  19. Chen B, Dai X, He B, Pan K, Li H, Liu X, et al. Differences in Staphylococcus aureus nasal carriage and molecular characteristics among community residents and healthcare workers at Sun Yat-Sen University, Guangzhou, Southern China. BMC Infect Dis. 2015;15(303):1–12.Google Scholar
  20. Askarian M, Zeinalzadeh A, Japoni A, Alborzi A, Memish ZA. Prevalence of nasal carriage of methicillin-resistant Staphylococcus aureus and its antibiotic susceptibility pattern in healthcare workers at Namazi hospital, Shiraz, Iran. Int J Infect Dis. 2009;13(5):241–7.View ArticleGoogle Scholar
  21. Saadatian-Elahi M, Tristan A, Laurent F, Rasigade JP, Bouchiat C, lle Ranc AG, et al. Basic rules of hygiene protect health care and lab workers from nasal colonization by Staphylococcus aureus: an international cross-sectional study. PLoS ONE. 2013;8(12):e82851.View ArticlePubMedPubMed CentralGoogle Scholar
  22. Gebreyesus A, Gebreselassie S, Mihret A. Nasal and hand carriage rate of methicillin resistant Staphylococcus aureus (MRSA) among health care workers in Mekelle hospital, North Ethiopia. Ethiop Med J. 2013;51(1):41–7.PubMedGoogle Scholar
  23. Abdel Rahman AT, Hafez SF, Abdelhakam SM, Ali-Eldin ZA, Esmat IM, Elsayed MS, et al. Antimicrobial resistant bacteria among HCWs in ICU at Ain Sham university hospitals. J Egypt Soc Parasitol. 2010;40(1):71–83.PubMedGoogle Scholar
  24. Pan SC, Tien KL, Hung IC, Lin YJ, Sheng WH, Wang MJ, et al. Compliance of health care workers with hand hygiene practices: independent advantages of overt and covert observers. PLoS ONE. 2013;8(1):e53746.View ArticlePubMedPubMed CentralGoogle Scholar
  25. Geofrey A, Abade A, Aboud S. Methicillin-resistant staphylococcus aureus (MRSA) colonization among intensive care unit (ICU) patients and health care workers at Muhimbili national hospital, Dar Es Salaam, Tanzania, 2012. Pan African Med J. 2015;21(211):1–9.Google Scholar
  26. Wang JL, Wang JT, Chen SY, Chen YC, Chang SC. Distribution of Staphylococcal cassette chromosome mec types and correlation with comorbidity and infection type in patients with MRSA bacteremia. PLoS ONE. 2010;5(3):e9489.View ArticlePubMedPubMed CentralGoogle Scholar
  27. Cirkovic I, Stepanovic S, Skov R, Trajkovic J, Grgurevic A, Larsen AR. Carriage and genetic diversity of methicillin-resistant Staphylococcus aureus among patients and healthcare workers in a Serbian university hospital. PLoS ONE. 2015;10(5):e0127347.View ArticlePubMedPubMed CentralGoogle Scholar
  28. Radhakrishna M, D’Souza M, Kotigadde S, Saralaya V, Kotian S. Prevalence of methicillin resistant Staphylococcus aureus carriage amongst health care workers of critical care units in Kasturba medical college hospital, Mangalore, India. J Clin Diagn Res. 2013;7(12):2697–700.Google Scholar
  29. Mihreta T, Shakya B, Shresth S. Nasal carriage of MRSA among a national medical college teaching hospital, Birgunj, Nepal. Nepal Med Coll. 2010;12(1):26–9.Google Scholar
  30. Widmer AF. Replace hand washing with use of a waterless alcohol hand rub? Clin Infect Dis. 2000;31(1):136–43. https://doi.org/10.1086/313888.View ArticlePubMedGoogle Scholar

Copyright

© The Author(s) 2018

Advertisement