ISSN: 0973-7510
E-ISSN: 2581-690X
, Gulbahar F. Karim2 , Asmaa M.S. Al-Bayati1 and Hiro Mohammed Obaid1The carriage of community-acquired methicillin-resistant S. aureus (CA-MRSA) has become a source of community-associated infections, particularly in the anterior nares of people worldwide. This study was aimed at determining the prevalence of community-acquired S. aureus (CA-SA) and CA-MRSA nasal carriage among healthy individuals of various ages in Kirkuk City and evaluating the susceptibility of isolates to various antibiotics. A total of 597 healthy individuals were recruited in the community between December 1, 2021, and December 30, 2022. Nasal swabs obtained from participants were taken to the laboratory, where bacteria were isolated and identified using phenotypic characteristics. The MRSA isolates were identified by applying the modified Kirby Bauer disc diffusion technique. The results showed that the prevalence of CA-SA and CA-MRSA nasal carriers was 16.6 and 4.5%, respectively. The average age of the participants was 33.2 years, with a male-to-female ratio of 1.1: 1. The highest resistance of the isolates was observed against oxacillin (27.3%), followed by penicillin G (24.3%), amoxicillin (15.2%), erythromycin (12.1%), and tetracycline (6.1%). There was a 9.1% resistance rate to clindamycin, rifampin, gentamycin, and ciprofloxacin. However, all CA-MRSA isolates were multi-drug resistant. However, all the isolates were sensitive (100 %) to vancomycin, linezolid, and mupirocin. The findings of the present study highlight the potential for CA-SA and CA-MRSA acquisition in this population, which may be related to antibiotic abuse or overuse as well as poor hygiene. To lessen the impact of community-associated strains of MRSA nasal carriage, this necessitates the probable need for infection prevention measures and adequate antibiotic therapy.
Prevalence, Staphylococcus aureus, MRSA Nasal Carriage, Antibiotic Resistant, CA-MRSA
Staphylococcus aureus is a human skin and mucosa commensal.1 It is a major pathogen found in both the community and hospitals that cause a variety of diseases,2 including recurrent tonsillitis,3 pneumonia, soft tissue infections, urinary tract infections, and bloodstream infections.2 Although S. aureus can colonize various parts of the human body, the anterior nares are the principal ecological niche for this bacterium. About 20-30% of people are permanent carriers, and about 30 % are transient carriers.4 Staphylococcus aureus has become resistant to some types of antibiotics. Methicillin-resistant S. aureus (MRSA) strains are spread worldwide and they were found to be resistant to various Beta-lactam (β-lactam) antibiotics such as penicillin, cephamycins, and cephalosporin,5 except ceftaroline (fifth-generation cephalosporins), which is used for treating MRSA infection.6 Also, the species of Staphylococcus often developed resistance to different classes of an antibiotic such as quinolones, macrolides, and aminoglycosides.5
The mecA gene, which encodes a penicillin-binding protein with a low affinity (PBP2a), is the genetic determinant of methicillin resistance in MRSA. The staphylococcal cassette chromosome mec (SCCmec) types IV and V, which are frequently carried by CA-MRSA, are the mobile genetic elements by which the mecA gene is transported.6 Since the 1990s, there has been an increase in CA-MRSA infections in the general population, and the incidence of S. aureus and MRSA is also rising rapidly.7,8 The nasal carriage rate of S. aureus has been frequently employed as an indicator for determining the antibiotic resistance of S. aureus and MRSA in the community because it is a significant risk factor for a wide range of staphylococcal infections.9 A research in Kirkuk, Iraq, found that 16% of 100 restaurant employees had MRSA nasal carriage.10 Additional research on CA-MRSA nasal carriage has been conducted in other regions of Iraq among a variety of populations, including healthy individuals in Diyala City,11 intermediate students in Muthanna Province,12 healthy children in Basrah City,13 Syrian refugees in Duhok City,14 and secondary school students at Duhok City.15 They demonstrated relative prevalence rates of 21.5, 24, 41.2, 35, and 2.04%, respectively. Similarly, a greater prevalence of MRSA nasal carriage (55/181) among the healthy population has been recorded in other countries, such as west Iran.16 Additionally, in a community-based study conducted in Arak, central Iran,17 Turkey,18 Jordan,19 and Saudi Arabia,20 the nasal colonization rates of MRSA were reported to be 4.5, 9, 40.9, and 25%, respectively. Screening enables the identification of nasal carriers, which enhances the application of decolonization and other preventive measures to reduce postoperative infection in carriers and the use of antibiotics.21,22
Therefore, the present study was conducted to determine the prevalence of CA-SA, including CA-MRSA nasal carriage, among a healthy population of all ages in Kirkuk City, Iraq. The antibiotic susceptibility of the test isolates was also detected.
This study was conducted between 1st December 2021 and 30th December 2022 among healthy people living in Kirkuk City. Ethical approval was obtained from the Ethics Committee of the College of Nursing, University of Kirkuk. A total of 597 individuals of both genders, with ages ranging from 10 to 70 years, participated in the study. An anonymous questionnaire that asked about socio-demographic information like age, gender, and whether or not the respondent had ever used antibiotics or been hospitalized within the previous three months was created. The study’s participants were chosen from a pool of community members. After giving their consent, approved by each participant or, in the case of minors (< 18 years old), by their parents on behalf of the minor, they were enrolled at their workplaces or homes.
Sample collection
Sterile cotton swabs were used for a biological sample collection from the anterior nares of all participants. The procedure was repeated after a month to demonstrate a persistent carrier of S. aureus, according to Azis et al.23 The samples were rapidly transported using Cary Blair transport media to the laboratory at the Department of Medical Laboratory Techniques, College of Health and Medical Techniques, Northern Technical University, Kirkuk, Iraq.
Microbiological analysis
The samples were cultured on 5% sheep blood agar and incubated at 37°C for 24-48 hr. The isolates were sub-cultured on mannitol salt agar, and nutrient agar, and then incubated at 37°C for 24-48 hr. Identification based on characteristics of colony features, gram staining reactions, and biochemical analysis including catalase, and coagulase tests (slide and tube methods) were used to identify S. aureus isolates according to previously described procedures.24 More so, the API-Staph system (Biomerieus, France) was employed for a confirmatory test.
Antimicrobial susceptibility testing
A suspension colony of each confirmed S. aureus isolate was made in sterile normal saline and cultured at 37°C for 15 minutes. The concentration was adjusted to 0.5% McFarland Standard. Then, using the modified disc diffusion (Kirby- Bauer) technique, the sensitivity of the test isolates was assessed against a variety of antibiotics, including penicillin (P; 10 µg), amoxicillin (AM; 10µg), oxacillin (OX; 1 µg), gentamycin (Gen; 10 µg), clindamycin (CD; 2 µg), rifampin (RM; 5 µg), erythromycin (E; 15 µg), ciprofloxacin (CIP; 5 µg), tetracycline (TE; 30 µg), linezolid (LZ; 30 µg), mupirocin (200; µg), and vancomycin (VA; 10 µg) obtained from Bioanalysis Company. The results of the antibiotic susceptibility patterns were interpreted according to the guidelines of the Clinical and Laboratory Standards Institute (CLSI).25 All oxacillin-resistant isolates were assessed as MRSA by their ability to grow on Muller Hinton agar containing (6 mg/ml) of oxacillin and 4% Nacl.26 Staphylococcus aureus strain (ATCC 25923) was used as a positive control to evaluate the effectiveness of microbiological and antibiotic sensitivity testing.27 D-test was used for detecting inducible clindamycin-resistant bacteria by placing clindamycin and erythromycin discs (Bioanalysis Company) on Muller-Hinton agar plates at a distance of 15 mm from each other and were incubated at 37°C for 24 hr. Clindamycin resistance is thought to be inducible when there is a flattening or D-shaped zone between the clindamycin and erythromycin discs.28 All tests were repeated three times.
Statistical analysis
All the data were collected and tabulated. The people who had recently taken antibiotics were removed. The association between the variables was examined using the Chi-Square test, and p < 0.01 was considered significant. The prevalence of nasal carriage of S. aureus as well as MDR-SA was calculated as a percentage of all participants who were positive at the anterior nares during the specific period of the study. Also, the percentage of resistant bacteria for each antibiotic was calculated.
A total of 597 healthy individuals were examined for S. aureus carriage using nasal swabs. Their ages ranged from 10 to 70 years, with a mean of 33.2 years. The ratio of male to female was 1.1:1. There was no statistical association between gender and CA-SA nasal carriage. Additionally, 99/597 (16.5%) persistent S. aureus carriers were identified because they produced positive results during both the first and second sample collection events, as shown in Tables 1 and 2. MRSA and MSSA were found to be present in 27/99 (27.3%) and 72/99 (72.7%) of the participants, which constitute 4.5 and 12%, respectively. The majority of CA-SA and CA-MRSA nasal carriages, which account for 3.69 and 1.17%, respectively, of all individuals, were also found among participants aged 21 to 30 years (Table 2). This result indicates a statistical association between age and CA-MRSA nasal carriage rate.
Table (1):
Events of sample collection (n=597).
Sampling event |
No. of CA-Nasal carriage S. aureus/Total |
% |
No. of CA-MRSA nasal carriage/ Total |
% |
|---|---|---|---|---|
1st Sampling |
102/597 |
17.1% |
27/597 |
4.5 |
2nd Sampling |
111/597 |
18.6% |
31/597 |
5.2 |
The positive samples at both 1st and 2nd. sample collection event |
99 /597 |
16.6% |
27/597 |
4.5 |
%: Percentage
Table (2):
Distribution of S. aureus and CA-MRSA nasal carriage based on age group and sex.
| Variable | No. (%) | S. aureus nasal carrying No. (%) | P- value | CA-MRSA nasal carriage No. (%) | P. value | |||
|---|---|---|---|---|---|---|---|---|
| Positive | Negative | Positive | Negative | |||||
| Age group (years) | ||||||||
| 10-20 | 240(40.20) | 18 (3.52) | 222 (37.19) | 0.00 | 03 (0.50) | 237 (39.70) | 0.001 | |
| 21-30 | 171(28.64) | 22 (3.69) | 149 (24.96) | 07 (1.17) | 164 (27.47) | |||
| 31-40 | 75 (12.51) | 20 (3.35) | 55 (9.21) | 05 (0.84) | 70 (11.73) | |||
| 41-50 | 36 (6.03) | 15 (2.52) | 21(3.52) | 03 (0.50) | 33 (5.53) | |||
| 51-60 | 45 (7.54) | 20 (3.35) | 25 (4.19) | 05 (0.84) | 40 (6.53) | |||
| 61-70 | 30 (5.03) | 04 (0.67) | 26 (4.36) | 04 (0.67) | 26 (4.36) | |||
| Total | 597 | 99 | 498(83.45) | 27(4.5) | 570 (95.48) | |||
| Gender | ||||||||
| Male | 315(52.76) | 54 (9.04) | 261( 43.72 ) | 0.697 | 15 (2.52) | 300 (50.25) | 0.766 | |
| Female | 282 (47.24) | 45(7.54) | 237 (39.7 ) | 12 (2.01) | 270 (45.23) | |||
| Total | 597 (100) | 99(16.6) | 498 (83.42) | 27 (4.5) | 570 (95.48) | |||
M: Male; F: Female; No.: Number: %: Percentage
Table (3):
Antibiotic resistant profile of nasal carriage S. aureus (n=99).
No. |
Antibiotics |
MRSA (n=27) |
% |
MSSA (n=72) |
% |
Total (n=99) |
% |
|---|---|---|---|---|---|---|---|
1 |
Penicillin G |
24 |
24.3 |
36 |
36.4 |
60 |
60.6 |
2 |
Oxacillin |
27 |
27.3 |
0 |
0 |
27 |
27.3 |
3 |
Amoxicillin |
15 |
15.2 |
09 |
9.1 |
24 |
24.2 |
4 |
Erythromycin |
12 |
12.1 |
06 |
6.1 |
18 |
18.2 |
5 |
Tetracycline |
06 |
6.1 |
06 |
6.1 |
12 |
12.1 |
6 |
Clindamycin |
09 |
9.1 |
03 |
3.0 |
12 |
12.1 |
7 |
Rifampin |
09 |
9.1 |
0 |
0 |
06 |
6.1 |
8 |
Gentamycin |
09 |
9.1 |
0 |
0 |
06 |
6.1 |
9 |
Ciprofloxacin |
09 |
9.1 |
03 |
3.0 |
06 |
6.6 |
10 |
Linezolid |
0 |
0 |
0 |
0 |
0 |
0 |
11 |
Mupirocin |
0 |
0 |
0 |
0 |
0 |
0 |
12 |
Vancomycin |
0 |
0 |
0 |
0 |
0 |
0 |
%: Percentage
As shown in Table 3, oxacillin resistance was found in 27/99 (27.3%) of the isolates, followed by penicillin G resistance in 24/99 (24.3%), amoxicillin resistance in 15/99 (15.2%), erythromycin resistance in 12/99 (12.1%), and tetracycline resistance in 6/99 (6.1%), and there was a 9/99 (9.1%) resistant rate to each of clindamycin, rifampin, gentamycin, and ciprofloxacin. When compared to methicillin-sensitive S. aureus (MSSA) isolates, it was observed that MRSA isolates have a greater resistance rate. Comparatively, all examined isolates were 100% (99/99) sensitive to vancomycin, linezolid, and mupirocin. Fifteen (2.51%) of the investigated isolates, including 9 MRSA and 3 MSSA, showed induced clindamycin resistance. Additionally, 27/99 (27.3%) of the isolates were MRSA, and 33/99 (33.3%) of them were multi-drug resistant. Multi-drug resistance, as used in this study, was defined as being resistant to three or more of the antimicrobial agents tested.
S. aureus is one of the most common opportunistic pathogens in the community and hospitals.2 Clinically important infections are frequently caused by it, and their severity can range from mild skin infections to more dangerous invasive illnesses.29 According to earlier studies, nearly 30% of healthy individuals are permanent nasal carriers of S. aureus, with a higher rate among children.30 MRSA strains in particular pose a significant risk for the development and subsequent insidious staphylococcal infections.31 In the current study, the prevalence of persistent nasal carriage of S. aureus among the population in Kirkuk City was 99/597 (16.6%). This observation is in line with that of other investigators in Marrakesh, who found that S. aureus was present in the anterior nares of 16.3% of 300 healthy children.32 The adult population of nine European countries was studied, and the prevalence of S. aureus was found to be greater (21.6%), ranging from 12.1% in Hungary to 29.4% in Sweden.33 Another study from the Iraqi province of Diyala also found a higher carriage rate than what was obtained in the present study, which was 21.5% out of 1186 healthy people.11 Moreover, the value obtained in the current study was found to be lower compared with previous studies in other areas of the world, such as Turkey,18 northwest Ethiopia,28 Iran,16 Italy,34 Nepal,35 which documented a carriage rate of 17, 23, 30.6, 42, 44, and 66%, respectively. In addition, the nasal carriage prevalence of S. aureus among specific groups, including healthcare workers in Erbil City,36 healthy children in Basrah City,13 secondary school students in Duhok City,15 workers in restaurants in Kirkuk City,10 were 24.5, 14.24, 18.4, and 30%, respectively. The variation of nasal carriage of S. aureus in the different investigations could be attributed to differences in geographical distribution, properties of the studied participants, sampling methodologies, preservation, and diagnostic methods.28 It has been reported that the mucin layer in the anterior nares is related to S. aureus colonization in this area of the body through an interaction of mucin carbohydrates with staphylococcal protein.37
MRSA nasal carriers were present in 4.5% of the study’s participants. This result is consistent with a community-based study from Arak, Iran.17 It was greater than the prevalence rate of CA-MRSA nasal carriage among secondary school children in Duhok City, Iraq, which was reported by previous researchers to be 2.04%.15 In other studies undertaken in Iraq, the nasal carriage prevalence of CA-MRSA among healthy children in Basrah City,13 intermediate students at Muthanna Province,12 and healthy workers in restaurants at Kirkuk City,10 were 41.2, 24, and 16%, respectively. Furthermore, the result of the current study is consistent with the reports from Italy,34 India,38 and Marrakesh,32 which showed that the prevalence of MRSA nasal carriage was 3, 3.17, and 4%, respectively. As opposed to reports from Egypt (32%), Saudi Arabia (25%),20 Africa (15%),28 Northwest Ethiopia (9.79%),28 and Jordan (40.9%),19 the prevalence of MRSA carriage in the present study was lower. The differences in the nasal carriage rate among these populations might be attributed to the initiation of antimicrobial therapy before sample collection.39 Furthermore, some research has discovered a link between S. aureus resistance to methicillin and the use of a beta-lactam combination.40
Concerning gender, the result of the current study showed that the percentage of male carriers was higher than that of females, but there was no statistical association between gender and MRSA carriage rate (p<0.01). This result is consistent with that reported by Abdelmalek et al.19 However, there is a significant statistical association between age and the CA-MRSA nasal carriage rate, as most CA-SA, and CA-MRSA nasal carriers were among the ages of 21 to 30 years, which constitute 3.69, and 1.17%, respectively, of all the participants. This observation might be attributed to attendance at a fitness center, as this practice is becoming very common in Iraq, particularly among males. This result is consistent with a recent study conducted in Jordan that examined the link between S. aureus carriage and gym attendance.19
Regarding antibiotic susceptibility, the majority of the studied isolates were resistant to oxacillin (27.2%), followed by penicillin G, 24/99 (24.3%), and amoxicillin, 15/99 (15.2%). The values obtained in this result were lower than those of other studies involving healthy individuals from the community, which showed high resistance to penicillin of about 65%,23 resistance to penicillin in Europe (87.1%),41 and resistance to penicillin in Nepal and Ohio (100%), with only 5.8 and 1.1% resistant rates to oxacillin in Nepal and Ohio, respectively.35 The resistance of S. aureus isolates to penicillin was determined within a decade after its introduction in 1940.42 As a result, new beta-lactam antibiotics were produced, which were related to the appearance of S. aureus strains that produce beta-lactamase.43 Since methicillin was developed to treat infectious disorders brought on by microbial strains resistant to penicillin, the occurrence of resistant S. aureus to methicillin has resulted in a decrease in the effectiveness of antibiotic therapy.44 Lower resistance of isolates was shown to exist against erythromycin (18.1%) and tetracycline (12.1%). Other studies also reported a low resistance (<12%) to both tetracycline and erythromycin, which is in line with the results obtained in the present study.23 Other investigators showed in a comparative study of two cities in Egypt and Saudi Arabia that a higher resistance rate to erythromycin was observed in selected MRSA and MSSA isolated from outpatients. Values of 55 and 24% were recorded for MRSA and MSSA, respectively, in Egypt and 58 and 25%, respectively, in Saudi Arabia.20 the percentage of resistance to clindamycin, rifampin, gentamycin, and ciprofloxacin was 9.1%. This observation was in line with other studies that reported low resistance of their S. aureus isolates and recorded high sensitivity of 94, 98, 90.2, 84 and 93% to clindamycin, gentamycin, cefoxitin, cotrimoxazole, and ciprofloxacin, respectively.28
Comparatively, all studied isolates (100%) were sensitive to vancomycin, linezolid, and mupirocin, indicating that these are appropriate treatments for MRSA infection and decontamination of MRSA carriers. This result is consistent with other findings in Basra, Iraq, that reported 100% susceptibility to vancomycin.45 In addition, other researchers from Erbil, Iraq, demonstrated that all isolates of MRSA and MASSA were susceptible to linezolid and mupirocin.36 The results also revealed that MRSA accounted for 27.3% of the isolates of S. aureus from healthy people’s anterior nares, which were 33.3% multi-drug resistant. This observation is slightly higher than another study, which reported 30.8%.28 Onanuga and Temedie, on the other hand, found that 52.5% of their isolates were multi-drug resistant community-associated S. aureus infections,46 of which were higher than the result of the present study. Moreover, 2.51% of isolates showed an inducible clindamycin-resistant phenomenon. This observation was lower than that reported by Baguma, who discovered that 42% of the test isolates showed this phenomenon.47 There are many recommendations for applying the PCR technique in the diagnosis of Methicillin-resistant Staphylococcus aureus48,49 due to their accurate results and short time. The polymerase chain reaction (PCR) was applied in the detection of pathogenic microorganisms,50-60 and genetic-related diseases.61-64
The findings from this study reveal that there is a chance that the population under study will develop community-associated S. aureus, MRSA, and multidrug resistance isolates, which may be caused by improper or excessive use of antibiotic therapy and poor hygiene. Additionally, it has been observed that MRSA isolates had a greater rate of antibiotic resistance than MSSA isolates during the investigation. This calls for prospective surveillance among local populations in various parts of the country, as well as molecular characterization of nasal carriage CA-MRSA to ascertain the prevalence and profile of antibiotic resistance among local communities across the country. Also, applying antimicrobial stewardship will help reduce the burden of antibiotic-resistant bacteria and community-associated MRSA nasal carriage infections.
ACKNOWLEDGMENTS
None.
CONFLICT OF INTEREST
The authors declare that there is no conflict of interest.
AUTHORS’ CONTRIBUTION
All authors listed have made a substantial, direct and intellectual contribution to the work, and approved it for publication.
FUNDING
None.
DATA AVAILABILITY
All datasets generated or analyzed during this study are included in the manuscript.
ETHICS STATEMENT
This study was approved by the Ethics Committee of the College of Nursing, University of Kirkuk, Kirkuk, Iraq.
INFORMED CONSENT
Written informed consent was obtained from the participants before enrolling in the study.
- Schmidt A, Benard S, Cyr S. Hospital cost of staphylococcal infection after cardiothoracic or orthopedic operations in France: A Retrospective Database Analysis. Surg infect. (Larchmt). 2015;16(4):428-435.
Crossref - David MZ, Daum RS. Community-associated methicillin-resistant Staphylococcus aureus: epidemiology and clinical consequences of an emerging epidemic. Clin Microbiol Rev. 2010;23(3):616-687.
Crossref - Karim GF, AL-Salihi SS, Atya QM, Abass KS. Aerobic and Anaerobic Bacteria in Tonsils of Different Ages with Recurrent Tonsillitis. Indian J Public Health Res Dev. 2019;10(9):1022-1026.
Crossref - Emaneini M, Jabalameli F, Rahdar H, Leeuwen WBV, Beigverdi R. Nasal carriage rate of methicillin resistant Staphylococcus aureus among Iranian healthcare workers: a systematic review and meta-analysis. Rev Soc Bras Med Trop. 2017;50(5):590-597.
Crossref - Iyer A, Kumosani T, Azhar E, Barbour E, Harakeh S. High incidence rate of methicillin-resistant Staphylococcus aureus (MRSA) among healthcare workers in Saudi Arabia. J Infect Dev Ctries. 2014;8(03):372-378.
Crossref - CLSI C. Performance standards for antimicrobial susceptibility testing. Clinical Lab Standards Institute. 2016;35(3):16-38.
- Cheung TK, Chu YW, Chu MY, Tsang VY, Lo JY. Panton-Valentine leukocidin-positive meticillin-resistant Staphylococcus aureus in the community in Hong Kong. J Med Microbiol. 2008;57(Pt 11):1440-1443.
Crossref - Seybold U, Kourbatova EV, Johnson JG, et al. Emergence of community-associated methicillin-resistant Staphylococcus aureus USA300 genotype as a major cause of health care-associated blood stream infections. Clin Infect Dis. 2006;42(5):647-656.
Crossref - Yamamoto T, Nishiyama A, Takano T, et al. Community-acquired methicillin-resistant Staphylococcus aureus: community transmission, pathogenesis, and drug resistance. J Infect Chemother. 2010;16(4):225-254.
Crossref - Mohammed MJ, Ali AA. Isolation of Staphylococcus aureus bacteria from nasal swabs from workers in restaurants in Kirkuk City. Int J Drug Delivery Technol. 2020;10:598-601.
- Hasan ARS, Al-Duliami AA, Abdul-Jabbar S. Nasal carriage of Staphylococcus aureus among healthy population in Diyala. Al-Nahrain Journal of Science. 2007;10(2):77-80.
Crossref - Hantoosh SM. Nasal Carriage of Vancomycin-and Methicillin-Resistant Staphylococcus aureus among Intermediate Students of Urban and Rural Schools of Muthanna Province in Iraq. Iraqi J Pharm Sci. 2022;31(1):102-108.
Crossref - Jamalludeen NM. Nasal Carriage of Staphylococcus Aureus in Healthy Children and its Possible Bacteriophage Isolates in Basrah, Iraq. Biomed Pharmacol J. 2021;14(1):467-475.
Crossref - Rasheed NA, Hussein NR. Prevalence of Nasal Carriage Rate and Antimicrobial Susceptibility Testing of Staphylococcus aureus Strains Isolated From Syrian Students in Kurdistan, Iraq. Middle East J Rehabil Health Stud. 2020;7(3):e103394.
Crossref - Habeeb A, Hussein NR, Assafi MS, Al-Dabbagh SA. Methicillin resistant Staphylococcus aureus nasal colonization among secondary school students at Duhok City-Iraq. J Microbiol Infect Dis. 2014;4(2):59-63.
Crossref - Khan-Mohammadi F, Kazemnia A, Beheshtipour J, Raeeszadeh M. Prevalence of and risk factors for methicillin-resistant Staphylococcus aureus nasal carriage in the West of Iran: a population-based cross-sectional study. BMC Infect Dis. 2019;19(1):89.
Crossref - Japoni-Nejad A, Rezazadeh M, Kazemian H, Fardmousavi N, van Belkum A, Ghaznavi-Rad E. Molecular characterization of the first community-acquired methicillin-resistant Staphylococcus aureus strains from Central Iran. Int J Infect Dis. 2013;17(11):e949-54.
Crossref - Demirel G, Findik D, Dagi HT, Arslan U. Community-acquired methicillin-resistant Staphylococcus aureus and genotypes among university students in Turkey. Southeast Asian J Trop Med Public Health. 2014;45(6):1401.
- Abdelmalek S, Qinna MW, Al-Ejielat R, Collier PJ. Methicillin-Resistant Staphylococci (MRS): carriage and antibiotic resistance patterns in college students. J Community Health. 2022;47(3):416-424.
Crossref - Abou Shady HM, Bakr AE A, Hashad ME, Alzohairy M. A. Staphylococcus aureus nasal carriage among outpatients attending primary health care centers: a comparative study of two cities in Saudi Arabia and Egypt. Braz J Infect Dis. 2015;19(1):68-76.
Crossref - Bode LG, Kluytmans JA, Wertheim HF, et al. Preventing surgical-site infections in nasal carriers of Staphylococcus aureus. N Eng J Med. 2010;362(1):9-17.
Crossref - Deeny SR, Cooper BS, Cookson B, Hopkins S, Robotham JV. Targeted versus universal screening and decolonization to reduce healthcare-associated meticillin-resistant Staphylococcus aureus infection. J Hosp Infect. 2019;85(1):33-44.
Crossref - Azis NM, Pung HP, Rachman ARA, et al. A persistent antimicrobial resistance pattern and limited methicillin-resistance-associated genotype in a short-term Staphylococcus aureus carriage isolated from a student population. J Infect Public Health. 2017;10(2):156-164.
Crossref - George MD, David RB, Richard WC. Berge’s Manual of Systemic Bacteriology. 2nd Edition, Springer, New York, 2001.
- CLSI (Clinical and Laboratory Standards Institute. Performance standards for antimicrobial susceptibility testing. CLSI supplement M 100. 2017.
- Alipour F, Ahmadi M, Javadi S. Evaluation of different methods to detect methicillin resistance in Staphylococcus aureus (MRSA). J Infect Public Health. 2014;7(3):186-191.
Crossref - Magiorakos AP, Srinivasan A, Carey RT, et al. Multidrug-resistant, extensively drug-resistant and pandrug-resistant bacteria: an international expert proposal for interim standard definitions for acquired resistance. Clin Microbiol Infect. 2012;18(3):268-281.
Crossref - Tigabu A, Tiruneh M, Mekonnen F. Nasal carriage rate, antimicrobial susceptibility pattern, and associated factors of Staphylococcus aureus with special emphasis on MRSA among urban and rural elementary school children in Gondar, Northwest Ethiopia: A comparative cross-sectional study. Adv Prev Med. 2018;11:9364757.
Crossref - Deng JJ, Xiao GG, Zhu Y, Zhou W, Wan C. Staphylococcus aureus nasal carriage and its antibiotic resistance profiles in Tibetan school children in Southwest China. HK J Paediatr. 2014;19(2):75-78.
- Shojaei H, Havaei SA, Koushki AM, Moghadasizadeh Z, Meidani M, Shirani K. Nasal colonization in children with community acquired methicillin-resistant Staphylococcus aureus. Adv Biomed Res. 2016;5:86.
Crossref - Huang FL, Ting PJ. Prevalence of and risk factors for nasal methicillin-resistant Staphylococcus aureus colonization among children in central Taiwan. J Microbiol Immunol Infect. 2019;52(1):45-53.
Crossref - Ed-dyb S, Aboudourib M, Azzouzi F, et al. Prevalence of Community Acquired Methicillin Resistant Staphylococcus aureus Nasal Carriage among Children of Consultation: Experience of a Moroccan University Hospital. J Arch Clin Microbiol. 2020;11(1):1-6.
Crossref - Hoffmann K, Apfalter P, Bartholomeeusen S, et al. Prevalence and resistance of commensal Staphylococcus aureus, including methicillin-resistant S aureus, in nine European countries: a cross-sectional study. Lancet Infect Dis. 2013;13(5):409-415.
Crossref - Mascaro V, Capano MS, Iona T, Nobile CGA, Ammendolia A, Pavia M. Prevalence of Staphylococcus aureus carriage and pattern of antibiotic resistance, including methicillin resistance, among contact sport athletes in Italy. Infect Drug Resist. 2019;12:1161-1170.
Crossref - Mahatara RL, Bempah S, Dhakal N, Smith TC. Multidrug-resistant Staphylococcus aureus Colonization in Healthy Adults Is more Common in Bhutanese Refugees in Nepal than Those Resettled in Ohio. Biomed Res Int. 2019;2019:5739247.
Crossref - Dogramachy NS. Prevalence of nasal carriage rate for methicillin-resistant Staphylococcus aureus and its antibiotic susceptibility profiles in health care workers at Nanakaly Hospital, Erbil, Iraq. Zanco J Med Sci. 2018;22(3):411-419.
Crossref - Peacock SJ, de Silva I, Lowy FD. What determines nasal carriage of Staphylococcus aureus? Trends Microbial. 2001;9(12):605-610.
Crossref - Shetty V, Trumbull K, Hegde A, Shenoy V, Prabhu R. Prevalence of community-acquired methicillin-resistant Staphylococcus aureus nasal colonization among children. J Clin Diagn Res. 2014;8(12):DC12-5.
Crossref - Breurec S, Zriouil SB, Fall C, et al. Epidemiology of methicillin-resistant Staphylococcus aureus lineages in five major African towns: emergence and spread of atypical clones. Clin Microbiol Infect. 2011;17(2):160-165.
Crossref - Sfeir M, Obeid Y, Eid C, et al. Prevalence of Staphylococcus aureus methicillin-sensitive and methicillin-resistant nasal and pharyngeal colonization in outpatients in Lebanon. Am J Infect Control. 2014;42(2):160-163.
Crossref - Zomer TP, Wielders CC, Veenman C, et al. MRSA in persons not living or working on a farm in a livestock-dense area: prevalence and risk factors. J Antimicrob Chemother. 2017;72(3):893-899. https://postprint.nivel.nl/PPpp6470.pdf
- Ventola CL. The antibiotic resistance crisis: part 1: causes and threats. Pharmacy and Therapeutics. 2015;40(4):277-283. PMID: 25859123
- Karimi M, Esfahani BN, Halaji M, et al. Molecular characteristics and antibiotic resistance pattern of Staphylococcus aureus nasal carriage in tertiary care hospitals of Isfahan, Iran. Infez Med. 2017;25(3):234-240. https://pubmed.ncbi.nlm.nih.gov/28956540/, MID: 28956540
- Oliveira D, Borges A, Simoes M. Staphylococcus aureus toxins and their molecular activity in infectious diseases. Toxins (Basel). 2018;10(6):252.
Crossref - Jasim HA, ALMoosawi WN. Nasal carriage of Staphylococcus aureus among Basra Medical students. Bas J Sci. 2014;32(2B):182-193. https://iasj.net/iasj/download/9df240e73b63689d
- Onanuga A, Temedie TC. Nasal carriage of multi-drug resistant Staphylococcus aureus in healthy inhabitants of Amassoma in Niger delta region of Nigeria. Afr Health Sci. 2011;11(2). https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3158512/,PMCID:PMC3158512,PMID: 21857847
- Baguma A, Musinguzi B, Mpeirwe M, Bazira J. Clindamycin resistance among methicillin resistant staphylococcus aureus isolated from human and respective household swine in greater Kabale Region-South Western Uganda. Adv Infect Dis. 2019;9(4):285-294.
Crossref - Fakhry SS, Hammed ZN, Bakir WA-E, ALRubaii BAL. Identification of methicillin-resistant strains of Staphylococcus aureus isolated from humans and food sources by use mecA 1 and mecA 2 genes in Pulsed-field gel electrophoresis technique. Bionatura. 2022;7(2):44.
Crossref - Ali M, Al-Rubaii B. Study of the Effects of Audible Sounds and Magnetic Fields on Staphylococcus aureus Methicillin Resistance and mecA Gene Expression. Trop J Nat Prod Res. 2021;5(5):825-830.
- Hashim ST, Fakhry SS, Rasoul LM, Saleh TH, Alrubaii BA. Genotyping toxins of Clostridium perfringens strains of rabbit and other animal origins. Trop J Nat Prod Res. 2021;5(4):613-616.
Crossref - Abdulkaliq Awadh H, Hammed ZN, Hamzah SS, Saleh TH, AL-Rubaii BA. Molecular identification of intracellular survival related Brucella melitensis virulence factors. Biomedicine. 2022; 42(4):761-765.
Crossref - Abdul-Gani MN, Laftaah BA. Purification and characterization of chondroitinase ABC from Proteus vulgaris, an Iraqi clinically isolate. Curr Sci. 2017:2134-2140.
Crossref - Kadhim AL-Imam MJ, AL-Rubaii BA. The influence of some amino acids, vitamins and anti-inflammatory drugs on activity of chondroitinase produced by Proteus vulgaris caused urinary tract infection. Iraqi J Sci. 2016; 57 (4A):2412-2421.
- Saleh, T.; Hashim, S.; Malik, S.N.; Al-Rubaii, B.A.L. The impact some of nutrients on swarming phenomenon and detection the responsible gene RsbA in clinical isolates of Proteus mirabilis. Int J Pharm Sci Res. 2020;1(6):437-444.
Crossref - Shehab ZH, Laftah BA. Correlation of nan1 (Neuraminidase) and production of some type III secretion system in clinical isolates of Pseudomonas aeruginosa. Biomed res. 2018;15(3):1729-1738.
- Al-Rubii, BAL. Cloning LasB gene of pseudomonas aeruginosa eiastase 10104-2aI in E. coli BL21 and E.coli DH5? and investigated their effect on the stripping of vero cells. Pakistan J Biotechnol. 2017;14(4):697-705.
- Abdulla L, Ismael MK, Salih TA, Malik SN, Al-Rubaii BA. Genotyping and evaluation of interleukin-10 and soluble HLA-G in abortion due to toxoplasmosis and HSV-2 infections. Ann Parasitol. 2022; 68(2):385-390.
- Jiad AL, Ismael MK, Muhsin SS, Al-Rubaii BA. ND2 Gene Sequencing of Sub fertile Patients Recovered from COVID-19 in Association with Toxoplasmosis. Bionatura. 2022; 7(3):45.
Crossref - Rasoul LM, Nsaif MM, Al-Tameemi MT, Al-Rubaii BA. Estimation of primer efficiency in multiplex PCR for detecting SARS-Cov-2 variants. Bionatura, 2022, 7(3): 48.
Crossref - Rasoul, LM., Marhoon AA, Albaayit SFA, Ali RW, Saleh,TH, Al-Rubaii BAL. Cytotoxic effect of cloned EGFP gene on NCI-H727 cell line via genetically engineered gene transfer system. Biomedicine (India). 2022, 42(5): 938-942.
Crossref - Ahmed AA, Khaleel KJ, Fadhel AA, Al-Rubaii BAL. Chronic Myeloid Leukemia: A retrospective study of clinical and pathological features. Bionatura, 2022, 7(3), 41.
Crossref - Ali SM, Lafta BA, Al-Shammary AM, Salih HS. In vivo oncolytic activity of non-virulent newcastle disease virus Iraqi strain against mouse mammary adenocarcinoma. AIP Conference Proceedings, 2021, 2372, 030010.
Crossref - Ali SM, Laftah BA, Al-Shammary AM, Salih HS. Study the role of bacterial neuraminidase against adenocarcinoma cells in vivo. InAIP Conference Proceedings 2021, 2372, 030009.
Crossref - Hamoode RH, Alkubaisy SA, Sattar DA, Hamzah SS, Saleh TH, Al-Rubaii BAL. Detection of anti-testicular antibodies among infertile males using indirect immunofluorescent technique. Biomedicine (India).2022; 42 (5):978-982.
Crossref
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