Research Article | Open Access
Mohammed Aljeldah1, Basim Al Shammari1, Eman S. Farrag1,Ehab M. Taha2 and Sabry Y. Mahmoud2
1Department of Clinical Laboratory Science, College of Applied Medical Sciences, University of Hafr Al Batin, Hafr Al Batin, Saudi Arabia.
2Biology Department, College of Science, Hafr Al Batin University, Hafr Al Batin, Saudi Arabia.
J Pure Appl Microbiol. 2022;16(2):1192-1199 | Article Number: 6838
https://doi.org/10.22207/JPAM.16.2.48 | © The Author(s). 2022
Received: 04/01/2021 | Accepted: 12/04/2022 | Published online: 31/05/2022
Issue online: June 2022
Abstract

Methicillin-resistant Staphylococcus aureus (MRSA) is responsible for serious threats to human health, causing various syndromes worldwide. Here, our purpose was to estimate the prevalence of nosocomial MRSA among isolates from King Khalid Hospital (KKH) and Maternity and Children Hospital (MCH) at Hafar Al-Batin Governorate, Saudi Arabia, and to determine the resistance of these isolates to common antibiotics used for treatment. One-hundred clinical specimens were collected from admitted patients during a six month period, and subjected to MRSA screening using traditional microbiological techniques. Antimicrobial susceptibility testing (AST) was also performed and confirmed by the VITEK2 automated system. Among the 37 S. aureus strains isolated from KKH, 23 (62.16%) were identified as MRSA. In MCH, 38 (60.31%) out 63 isolated strains were identified as MRSA. According to AST, few MRSA strains were resistant to teicoplanin, fosfomycin, linezolid, and mupirocin in both hospitals. Vancomycin resistance was not detected in any of the MRSA strains. Twelve MRSA strains from KKH and 17 strains from MCH were considered multidrug resistant (MDR). In conclusion, prevention is critical to reduce the high prevalence of MRSA.

Keywords

Staphylococcus aureus, MRSA, multidrug-resistant, prevalence, Saudi Arabia

Introduction

S. aureus is one of the most important nosocomial pathogenic agents worldwide. It can cause a wide range of infections, especially meningitis, endocarditis, and bloodstream infections, which are often fatal in nature.1 S. aureus infections are particularly difficult to treat due to increased resistance to antimicrobial drugs. Methicillin-resistant S. aureus (MRSA) has become the world’s leading source of antimicrobial-resistant health care-associated infections (European Centre for Disease Prevention and Control).2

Many MRSA isolates become multidrug-resistant (MDR), which are only susceptible to glycopeptide antibiotics such as vancomycin.3 Possible risk factors involved in the acquisition of MDR-MRSA emergence include the use of antibiotics, lack of knowledge, being on antibiotics before arriving to the hospital, prolonged hospitalization, and indiscriminate.4 MRSA infections are now widespread and epidemic in hospitals and long-term health facilities worldwide, and the distribution of these isolates allows further transmission.5,6 This emphasizes the need to consider the prevalence of MRSA and its antimicrobial profile to select effective empirical treatments and control measures.

In Saudi Arabia, the prevalence of MRSA among S. aureus isolates varies widely across regions and has shown temporal increases. Low MRSA prevalence (5–7.5%) was regularly observed in the early 1990s, rising dramatically to 91% after 1995.7 The average prevalence of MRSA in Saudi Arabia was 29.9% from January 1990 to April 2011.8 Recently, the overall Saudi MRSA prevalence rate was 35.6% from a pooled estimate of 22,793 S. aureus strains collected between 2002 and 2012.9

The present study was conducted to estimate the preva¬lence of MRSA isolates from Hafar Al-Batin hospitals and determine their antimicrobial resistance profiles.

Materials and Methods

A total of 100 non-replicate clinical strains of S. aureus were isolated from various specimens of patients admitted to the King Khalid Hospital (KKH) and Maternity and Children Hospital (MCH), Hafar Al-Batin, Eastern Region, Saudi Arabia between July 2019 and December 2019. The sources of the strains were pus, blood, urine wound swab, purulent discharge, sputum, ear swab, nasal swab, throat swap, abscesses, catheter tip, and suction tip, which were obtained from patients who had been hospitalized for more than 48 h. Ethical approval was obtained from the Institutional Review Board (IRB) committee of Hafar Al-Batin (approval Number: 67) and the committee registration with King Abdulaziz City for Science and Technology (KACST), Kingdom of Saudi Arabia (No. H-05-FT-083).

All clinical specimens were cultured on blood agar and mannitol salt agar plates and incubated at 35°C for 24 to 48 h. Isolated bacteria were identified according to colonial and microscopic morphology, Gram staining, as well as catalase, coagulase (using rabbit plasma), Slidex Staph plus (SSP) latex reagent (bioMerieux France), DNase, and Mannitol fermentation tests.10 All isolates positive for these tests were identified as S. aureus.

Based on the Clinical Laboratory Standards Institute guidelines,11 all S. aureus isolates were tested for methicillin resistance using oxacillin screen agar and cefoxitin disc diffusion tests. Furthermore, the Kirby Bauer Disc Diffusion test has been introduced for routine antimicrobial susceptibility testing (AST) of traditional and recently introduced antibiotics based on CLSI recommendations (2012 and 2014). The VITEK 2 automated system was used to confirm the results of strain identification and AST according to the instructions of the manufacturer (bioMerieux France).

MRSA incidence was calculated as: total number of intermediate and resistant isolates/total number of isolates. Isolates resistant to penicillin, oxacillin, and cefoxitin plus three or more classes of the antibiotics used in this study were considered MDR.12 Antimicrobial susceptibility rates are presented with 95% confidence interval values.

All data were examined using iBM SPSS version 21.0. Frequencies were calculated for categorical variables. The Chi-square test was used to analyze significant differences at a 95% confidence level. Statistical significance was set at p < 0.01, unless otherwise noted.

RESULTS AND DISCUSSION

The regular surveillance of hospital-acquired MRSA infection is a very effective procedure in assisting the monitoring of antibiotic policies. In this study, wounds were the most common site of infection (46 specimens). In 30 of them, MRSA was the causative agent. This finding confirmed that skin and soft tissue infections are the main reservoir of MRSA. Previous studies have shown a higher prevalence in skin infections inside and outside the hospital than in other sites of infection.13

Of the 100 clinical S. aureus isolates reported in the present study, 63 were isolated from MCH, while 37 were recovered from KKH. Different clinical specimens were collected from both hospitals (Table 1). Wound swabs represented most of the collected specimens (46), followed by abscesses, blood, pus, as well as suction and catheter tips (10). Low numbers of specimens were obtained from purulent discharge (3) as well as urine, sputum, and ear, nasal, and throat swabs (1). In a recent European study, the most common species in skin and soft tissue infections was S. aureus (71% of cases), with 22.5% being MRSA.14 In Saudi Arabia, S. aureus was shown to be the most common cause of infection in wounds, skin, and soft tissue, and these sites also showed the highest prevalence of MRSA.15,16 Al-Hamad et al. found that the vast majority of MRSA isolates collected in Qatif from 2006 to 2015 were obtained from wound and pus specimens.17

Table (1):
Distribution of MRSA among clinical specimens (n= 100) collected from King Khalid (KKH) and Maternity and children hospital (MCH).

Specimen (n) KKH MCH
No. MRSA No. MRSA
Pus (10) 1 1 9 5
Blood (10) 10 6
Urine (1) 1 0
Wound (46) 14 8 32 22
Purulent discharge (3) 3 1
Sputum (1) 1 1
Ear (1) 1 1
Nasal (6) 6 3
Throat (2) 2 1
Abscesses (10) 10 7
Suction and Catheter (10) 7 5 3 0
Total 37 23 63 38

Of the 100 clinical S. aureus isolates from both hospitals, 61 were identified as MRSA (23 out of 37 (62.16%) from KKH, and 38 out of 63 (60.31%) from MCH. Thirty MRSA isolates (49.1%) were isolated from wound swabs, while 6 (9.8%) were isolated from pus and blood specimens.

The antibiotic susceptibility data for MRSA and methicillin-susceptible S. aureus (MSSA) are summarized in Table 2. MRSA isolates had higher resistance rates to various antibiotics than MSSA isolates. Resistance to cefoxitin (30 μg-1), oxacillin (8 μg-1), and penicillin (10 μg-1) was found in all MRSA isolates (100%). In contrast, no MRSA strains resistant to vancomycin were isolated from either of the hospitals.

Table (2):
Antibiotics resistance pattern of MRSA (n=23) and MSSA (n=14) isolates from King Khalid hospital.

Antibiotics   Sensitivity (%) CI Resistance (%) CI
Cefoxitin MRSA 0  (0.0) 0.00-0.14 23 (100) 0.86-1.00
MSSA 14 (100) 0.78-1.00 0   (0.0) 0.00-0.22
Clindamycin MRSA 10 (43.5) 0.26- 0.63 13 (56.5) 0.37-0.74
MSSA 10 (71.4) 0.45-0.88 4   (28.6) 0.12-0.55
Erythromycin MRSA 9   (39.1) 0.22- 0.59 14 (60.9) 0.41-0.78
MSSA 10 (71.4) 0.45-0.88 4   (28.6) 0.12-0.55
Fosfomycin MRSA 22 (95.7) 0.76- 0.99 1   (4.3) 0.01-0.21
MSSA 13 (92.9) 0.69-0.99 1   (7.1) 0.013-0.31
Fusidic Acid MRSA 12 (52.2) 0.33-0.71 11 (47.8) 0.27-0.67
MSSA 11 (78.6) 0.52-0.92 3   (21.4) 0.08-0.48
Gentamicin MRSA 18 (78.3) 0.58- 0.90 5   (21.7) 0.09-0.42
MSSA 14 (100) 0.78-1.00 0   (0.0) 0.00-0.22
Levofloxacin MRSA 18 (78.3) 0.58- 0.90 5   (21.7) 0.09-0.42
MSSA 10 (71.4) 0.45-0.88 4   (28.6) 0.12-0.55
Linezolid MRSA 20 (87) 0.68-0.95 3   (13.0) 0.05-0.32
MSSA 14 (100) 0.78-1.00 0   (0.0) 0.00-0.22
Moxifloxacin MRSA 16 (69.6) 0.49-0.84 7   (30.4) 0.16-0.51
MSSA 10 (71.4) 0.45-0.88 4   (28.6) 0.12-0.55
Mupirocin MRSA 20 (87) 0.68-0.95 3   (13.0) 0.05-0.32
MSSA 14 (100) 0.78-1.00 0   (0.0) 0.00-0.22
Oxacillin MRSA 0  (0.0) 0.00-0.14 23 (100) 0.86-1.00
MSSA 14 (100) 0.78-1.00 0   (0.0) 0.00-0.22
Penicillin MRSA 0  (0.0) 0.00-0.14 23 (100) 0.86-1.00
MSSA 14 (100) 0.78-1.00 0   (0.0) 0.00-0.22
Rifampin MRSA 21 (91.3) 0.73-0.98 2  (8.7) 0.02-0.27
MSSA 13 (92.9) 0.69-0.99 1  (7.1) 0.01-0.31
Teicoplanin MRSA 22 (95.7) 0.79-0.99 1  (4.3) 0.01-0.21
MSSA 14 (100) 0.78-1.00 0 (0.0) 0.00-0.22
Tetracycline MRSA 15 (65.2) 0.45-0.81 8 (34.8) 0.19-0.55
MSSA 14 (100) 0.78-1.00 0 (0.0) 0.00-0.22
Trimeth/Sulfa MRSA 20 (87) 0.68-0.95 3 (13.0) 0.05-0.32
MSSA 14 ( 100) 0.78-1.00 0 (0.0) 0.00-0.22
Vancomycin MRSA 23 (100) 0.86-1.00 0 (0.0) 0.00-0.14
MSSA 14 (100) 0.78-1.00 0 (0.0) 0.00-0.22

CI = Confidence Interval

MRSA has become an enormous problem because it is hardly treated and develops resistance.18 During the six months examined in this study, the prevalence of MRSA was 62.2% in KKH and 60.31% in MCH. These values are very high compared with those of previous reports from other hospitals in Saudi Arabia.18 This could be attributed to the special environmental and host factors at Hafar Al-Batin, which is a border town near Iraq, Kuwait, and Jordan. MRSA incidence varies across Saudi Aria and is therefore not uniform. Low MRSA occurrence (5–7.5%) was regularly found in the early 1990s, rising drastically to 91% after 19957. In Saudi Arabia, the mean prevalence of MRSA was 29.9% from January 1990 to April 20118. A study conducted in 2013 compiled information on MRSA in Saudi Arabia between 2002 and 2012, covering five regions (Makkah, Dahran, Riyadh, Assir, and Al-Gouf) and including 26 published research articles. This study concluded that 35.6% of the 22,793 strains of S. aureus were MRSA (95% CI, 0.28–0.42; P < 0.01).9 In Saudi Arabia’s Eastern Zone (Al-Sharqia), the prevalence of MRSA has continued to vary. MRSA prevalence was reported to be 2.3% in Al-Hasa,18 5.9% in Daharan,19 and 38.4–47.2 % in Al-Khobar.20,21 Nevertheless, the proportion of MRSA was 22.1% and 24% in Daharan and Al-Ahsa, respectively.22,23 In contrast, other studies from regional countries have shown higher MRSA prevalence (>50% in Jordan, Egypt, and Cyprus).24 MRSA prevalence was shown to be 13.2% in Qatar and 32% in Kuwait.25,26 At an international scale, MRSA incidence also varies greatly between countries (e.g., 54.6% in Portugal versus 38.2% in Italy and 1.2% Denmark) (European Centre for Disease Prevention and Control)2.

In this study, resistance to other antibiotics greatly varied between the two hospitals (Tables 2 and 3). In KKH, MRSA showed lower resistance rates to fosfomycin and teicoplanin (one isolate; 4.3%), rifampin (two isolates; 8.7%) as well as linezolid, mupirocin, and trimethoprim/sulfamethoxazole (3 isolates each; 13%). Resistance to other antibiotics differed, and greater resistance to erythromycin, clindamycin, fusidic acid, tetracycline, and moxifloxacin was found. All MRSA strains in MCH were susceptible to fosfomycin, linezolid, moxifloxacin, mupirocin, teicoplanin, and tetracycline, while most isolates showed resistance to rifampicin and fusidic acid (35 (92.1%) and 25 (65.8%), respectively).

Table (3):
Antibiotics resistance pattern of MRSA (n=38) and MSSA (n=25) isolates from Maternity and children hospital.

Antibiotics   Sensitivity (%) 95% CI Resistance (%) 95% CI
Cefoxitin MRSA 0   (0.0) 0.00-0.09 38 (100) 0.91-1.00
MSSA 25 (100) 0.87-1.00 0   (0.0) 0.00-0.13
Clindamycin MRSA 29 (76.3) 0.61-0.87 9   (23.7) 0.13-0.39
MSSA 24 (96.0) 0.80-0.99 1   (4.0) 0.01-0.19
Erythromycin MRSA 29 (76.3) 0.61-0.87 9   (23.7) 0.13-0.39
MSSA 18 (72.0) 0.52-0.86 7   (28.0) 0.14-0.48
Fosfomycin MRSA 38 (100) 0.91-1.00 0   (0.0) 0.00-0.09
MSSA 25 (100) 0.87-1.00 0   (0.0) 0.00-0.13
Fusidic Acid MRSA 13 (34.2) 0.21-0.50 25 (65.8) 0.49-0.79
MSSA 21 (84.0) 0.65-0.94 4   (16.0) 0.06-0.35
Gentamicin MRSA 35 (92.1) 0.79-0.97 3   (7.9) 0.03-0.21
MSSA 24 (96.0) 0.80-0.99 1   (4.0) 0.01-0.19
Levofloxacin MRSA 36 (94.7) 0.83-0.99 2   (5.3) 0.01-0.17
MSSA 23 (92.0) 0.75-0.98 2   (8.0) 0.02-0.25
Linezolid MRSA 38 (100) 0.91-1.00 0   (0.0) 0.00-0.09
MSSA 25 (100) 0.87-1.00 0   (0.0) 0.00-0.13
Moxifloxacin MRSA 38 (100) 0.91-1.00 0   (0.0) 0.00-0.09
MSSA 24 (96.0) 0.80-0.99 1   (4.0) 0.01-0.19
Mupirocin MRSA 38 (100) 0.91-1.00 0   (0.0) 0.00-0.09
MSSA 25 (100) 0.87-1.00 0   (0.0) 0.00-0.13
Oxacillin MRSA 0   (0.0) 0.00-0.09 38 (100) 0.91-1.00
MSSA 25 (100) 0.87-1.00 0   (0.0) 0.00-0.13
Penicillin MRSA 0   (0.0) 0.00-0.09 38 (100) 0.91-1.00
MSSA 25 (100) 0.87-1.00 0   (0.0) 0.00-0.13
Rifampin MRSA 3   (7.9) 0.03-0.21 35 (92.1) 0.79-0.97
MSSA 0   (0.0) 0.00-0.13 25 (100) 0.87-1.00
Teicoplanin MRSA 38 (100) 0.91-1.00 0   (0.0) 0.00-0.09
MSSA 25 (100) 0.87-1.00 0   (0.0) 0.00-0.13
Tetracycline MRSA 38 (100) 0.91-1.00 0   (0.0) 0.00-0.09
MSSA 23 (92.0) 0.75-0.98 2   (8.0) 0.02-0.25
Trimeth/Sulfa MRSA 36 (94.7) 0.83-0.99 2   (5.3) 0.01-0.17
MSSA 22 ( 88.0) 0.70-0.96 3   (12.0) 0.04-0.29
Vancomycin MRSA 38 (100) 0.91-1.00 0   (0.0) 0.00-0.09
MSSA 25 (100) 0.87-1.00 0   (0.0) 0.00-0.13

CI = Confidence Interval

This study demonstrated that approximately half of the MRSA strains isolated from KKH and MCH were MDR (52.2 and 44.7%, respectively), with considerable variation in the antibiotics to which they were resistant. Vancomycin was the most effective agent, followed by teicoplanin, fosfomycin, linezolid, and mupirocin, in both hospitals (Tables 2–4). Resistance to β-lactam and closely related antibiotics may be caused by the production of beta-lactamase (an enzyme that inactivates the β-lactam ring).27 The most common reason for the development of multi-drug resistant MRSA is the indiscriminate use of antibiotics without drug sensitivity testing.28 Many studies conducted in Saudi Arabia have reported similar data, with MDR-MRSA rates of 85.2%,29 55%,30 and 32.14%.31 The first-line prescription for MRSA treatment has been vancomycin.32,33 However, vancomycin use should be limited to MRSA infections for which other medications are not suitable.

Table (4):
MRSA Resistant patterns and multidrug-resistant from King Khalid Hospital (n=12) and Maternity and children hospital (n=17).

Location Antibiotic resistance pattern (n) Antibiotics which are resistant No. of MRSA
KKH R1 (6) CE, OX, PE, CL, ER, MO 1
R2 (6) CE, OX, PE, CL, ER, LI 1
R3 (6) CE, OX, PE, CL, ER, FU 1
R4 (7) CE, OX, PE, CL, ER, GM, LI 1
R5 (7) CE, OX, PE, ER, LE, MO, TE 1
R6 (7) CE, OX, PE, ER, LE, MO, FU 1
R7 (8) CE, OX, PE, CL, ER, FU, MU, TE 1
R8 (9) CE, OX, PE, ER, GM, LE, MO, TE, TR 1
R9 (10) CE, OX, PE, CL, ER, FU, GM, LE, MO, RA 1
R10 (10) CE, OX, PE, CL, ER,  FU, GM, RA, TE, TR 1
R11 (11) CE, OX, PE, CL, ER, FU, LE, MO, MU, TE, TR 1
R12 (12) CE, OX, PE, CL, ER, FO, FU, GM,  LI, MU, TE, TE 1
MCH R1 (6) CE, OX, PE, RA, MO, LE 1
R2 (6) CE, OX, PE, RA, FU, TE 4
R3 (6) CE, OX, PE, RA, CL, ER 2
R4 (6) CE, OX, PE, RA, FU, GM 3
R5 (7) CE, OX, PE, RA, FU, CL, ER 6
R6 (9) CE, OX, PE, RA, FU, CL, ER, LE,TR 1

CE- Cefoxitin, CL-  Clindamycin, ER- Erythromycin, FO-  Fosfomycin, FU- Fusidic Acid, GM- Gentamicin, LE-  Levofloxacin, LI- Linezolid, MO- Moxifloxacin, MU- Mupirocin, OX- Oxacillin, PE- Penicillin, RA-Rifampin, T- Teicoplanin, TE-Tetracycline, TR- Trimeth/Sulfa, VA- Vancomycin. King Khalid Hospital, KKH; Maternity and children hospital, MCH.

Antibiotic susceptibility patterns and MDR are summarized in Table 4. Twelve MRSA strains (52.2%) from KKH and 17 (44.7%) from MCH harbored resistance to three or more antimicrobials as well as penicillin, oxacillin, and cefoxitin. There was considerable variation in antibiotic resistance patterns between the two hospitals. Twelve different patterns were shown from KKH, with a high number of antibiotics to which the isolates were resistant (6–12 antibiotics). MCH showed only 6 patterns, with a lower number of antibiotics to which they were resistant (6–9 antibiotics).

CONCLUSION

In conclusion, our findings demonstrate that MRSA is a serious problem in Saudi Arabia. Compared with MSSA isolates, MRSA isolates showed a higher prevalence of multidrug resistance. Vancomycin remains the mainstay treatment for MRSA infections. The rise in MDR-MRSA prevalence emphasizes the importance of sound infection treatment in hospitals.

Declarations

ACKNOWLEDGMENTS
The authors extend their appreciation to the Deanship of Scientific Research at the University of Hafr Al-Batin for funding this work.

CONFLICT OF INTEREST
The authors declare that there is no conflict of interest.

AUTHORS’ CONTRIBUTION
All authors designed the experiments. ESF, EMT and SYM performed the experiments. MA, ESF and BA analyzed the data. EMT and SYM wrote the manuscript. All authors read and approved the manuscript for final publication.

FUNDING
This research was funded by the Deanship of Scientific Research, Hafr Al-Batin University, Saudi Arabia under grant no. RGP-S-0012-1443.

ETHICS STATEMENT
This study was approved by the Institutional Ethics Committee, King Khalid Hospital (KKH), and Maternity and Children Hospital (MCH), Hafr Al-Batin, Saudi Arabia with reference number:  KACST No. H-05-FT-083.

AVAILABILITY OF DATA
All datasets generated or analyzed during this study are included in the manuscript.

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