Nasal Carriage Rate Of Staphylococcus aureus, Associated Factor And Its Antibiotic Susceptibility Patterns Among Students Of Collage Of Health And Medical Science WITH Clinical Attachment

doi:10.21203/rs.3.rs-4202805/v1

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Nasal Carriage Rate Of Staphylococcus aureus, Associated Factor And Its Antibiotic Susceptibility Patterns Among Students Of Collage Of Health And Medical Science WITH Clinical Attachment

https://doi.org/10.21203/rs.3.rs-4202805/v1

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Background: Staphylococcus aureus infections, including methicillin-resistant strains, are increasing globally. Medical students are at a higher risk of contracting this pathogen due to their close contact with health facilities during their clinical attachments. Limited studies exist in Harar, Eastern Ethiopia.

Objective: to assess the nasal carriage rate of S. aureus, associated factors, and antibiotic susceptibility patterns among students of Haramaya University, College of Health and Medicine Sciences students with clinical attachment, Harar Eastern Ethiopia from July 01 to August 30, 2022.

Methods: An institution-based cross-sectional study was carried out on 250 study participants using a stratified random sampling method. Data were collected via structured questionnaires. Nasal swabs were cultured on Mannitol Salt Agar and Blood Agar at 37°C for 24 hours. Staphylococcus aureus was identified using catalase and coagulase tests. Methicillin-resistant Staphylococcus aureus was screened using the Cefoxitin disk diffusion method on Muller Hinton agar. The data was entered and analyzed by SPSS version 25 software. Chi-square test was used to determine factors associated with the nasal carriage of Methicillin-resistant staphylococcus aureus. A p-value < 0.05 was considered statistically significant.

Results: In this study, Staphylococcus aureus prevalence was 8% (95% CI: 4.6%-11.3%) and Methicillin-resistantStaphylococcus aureus prevalence was 4.8% (95% CI: 2.1%-7.4%) among 250 participants. Significant factors for Methicillin-resistant Staphylococcus aureus nasal carriage included nose-picking habit (P=0.001) and dormitory student count (P=0.05). MRSA strains displayed high resistance, with 100% resistance to Ampicillin and Penicillin, 66.7% to Tetracycline, 25% to Erythromycin and Ciprofloxacin, 16% to Co-trimoxazole and Gentamicin. Chloramphenicol and Clyndamycin showed complete susceptibility.

Conclusion: The study reveals significant MRSA prevalence with resistance to common antibiotics. Nasal carriage associates with nose-picking and dormitory size. Enhanced hygiene education and stringent antibiotic stewardship are recommended to mitigate MRSA spread, particularly in communal living environments.

Clinical Students

Methicillin-resistant Staphylococcus aureus

Nasal carriage

Staphylococcus aureus.

Staphylococcus aureus (S.aureus) is a bacteria most healthy people have on their skin and nasal mucosa. The anterior nares are the most common sites of S. aureus colonization in humans. This acts as a reservoir for the pathogens (Williams, 1963). This bacteria can establish solid interactions with nasal epithelial cells via various proteins and many cell surface components (Sakr et al., 2018). It is a common cause of clinically significant infections, which range in severity from minor infections to severe invasive illnesses (Tigabu et al., 2018).

In healthy people, S.aureus nasal carriage patterns include persistent carriage, intermittent carriage, and non-carriage. Longitudinal studies show that about 20% (range 12–30%) of people are persistent S.aureus nasal carriers, and 30% (range 16–70%) are intermittent carriers. Since 2000, based on cross-sectional surveys of healthy adult populations have revealed S.aureus nasal carriage rates of around 27% (Wertheim et al., 2005).

Carriage of S. aureus in the nose has been associated with numerous factors, and it appears to play an important role in the pathogenesis of infection (Von Eiff et al., 2001). S.aureus colonization was related to diabetes mellitus, chronic obstructive pulmonary disease (COPD), stroke, and antibiotic medication within the previous three months (Daeschlein et al., 2006). Methicillin-resistant Staphylococcus aureus is a strain of S.aureus that has developed resistance to β-lactam antibiotics such as Methicillin, Oxacillin, Cefoxitin and Nafcillin (Reta et al., 2019). Medical students make up a significant portion of the healthcare workforce. They are infected with S.aureus as a result of the use of gloves when handling patients, the length of their hospital stay, and their habit of nose picking, Maintain only a moderate level of hand sanitization, Ward rotations and the sharing of personal belongings (Treesirichod et al., 2013) (Mekuriya et al., 2022c). Methicillin-resistant Staphylococcus aureus is a common cause of infections in hospitals and communities around the world (Köck et al., 2010).

Asymptomatic S. aureus carriage in healthy individuals is common, particularly in healthcare workers (Bradley, 1999).

Medical students are an important part of the healthcare workforce because they have frequent contact with the community in general and the healthcare environment in particular. In addition, they live in dormitories sharing spaces with other students in a kind of crowded living setting which widens the probability of acting as a vehicle for multidrug-resistant bugs like MRSA (Stevens et al., 2010). Therefore, this study is conducted to determine the nasal carriage rate of MRSA, its associated factors and antibiotic susceptibility patterns among students of Haramaya University, College of Health and Medicine Sciences (HUCHMS) with clinical attachment, Harar, Ethiopia.

Study Area and Period

The study was carried out in HUCHMS from July 01 to August 30, 2022, located in Harar town, 526 km from the capital city, Addis Ababa. HUCHMS is organized for the School of Medicine, School of Pharmacy, School of Nursing and Midwifery, school of medical laboratory science, school of public health and environmental health department. Currently, the college has a total of 1754 students in undergraduate and post-basic programs (regular).

Study Design, Period and Population

An institutional-based cross-sectional study was conducted. The source population was all students in HUCHMS with clinical attachment and all students selected from each department at HUCHMS with clinical attachment were sample population.

Eligibility Criteria

All HUCHMS Students without a history of hospitalization in the preceding six months and those who voluntarily participated were included. Those who had nasal infections and bleeding, any sign of clinical illness during the study period, received intranasal antibiotic ointment or other antibiotics within the previous two weeks of the commencement of the study were excluded.

Sample size determination and sampling technique

The sample size was determined by a single population proportion formula using the prevalence of nasal carriage of MRSA from a study conducted at Arbaminch University, Medical College with a Z score for a 95 confidence interval of 1.96, a margin of error of 5%, Since there is a small population of students with clinical attachment in the campus (N = 909), reduction formula was used and 10% non-response rate was added. The final sample size was 250.

Then, this sample size was allocated proportionally to each department and then batches within the departments. Finally, a simple random sampling technique was used to select the participants. The randomness of the sample was ensured by using a lottery method.

Data Collection Instruments and Procedures

A structured questionnaire was used to collect data. The questionnaire contains two parts: the first was socio-demographic variables like age, gender, department and year of education, and the second part contains possible risk factors associated with the colonization of MRSA like personal hygiene such as washing hands upon arriving at the hospital, hand washing after handling every patient contact, hand washing before and after meals, while leaving the hospital, alcohol use, frequency of hand washing with soap, use of gloves while handling patients, sharing of materials, habit of smoking cigarette, nose picking habit, number of students in one dormitory hospital exposure duration, if there is admission to ICU, presence or history of having indwelling device, history of hospitalization, history of chronic disease, ways of antibiotic usage, participate in invasive procedures. Which were developed from different kinds of literature (Mekuriya et al., 2022a, Efa et al., 2019a)

Specimen collection and Transportation

Nasal swab specimens were Self-sampled by using sterile cotton tip swabs pre-wetted with sterile saline for participants’ anterior nares into a depth of about 1cm and rotating it against the interior surface of the nostril. Then the swabs were inserted into the Amies transport medium (Oxoid, UK), and transported to the Microbiology laboratory of HUCHMS by maintaining a cold chain.

Laboratory Isolation and Identification

The nasal swabs were inoculated on Mannitol Salt Agar (MSA) (Oxiod, UK) and blood agar then incubated at 37 C for 24 hours. All isolates that shown complete hemolysis on blood agar plate and golden-yellow colonies on MSA, coupled with positive reaction for Gram stain, Catalase and DNase test were then considered as S. aureus (Zurita et al., 2010, Humphries et al., 2021).

Antimicrobial Susceptibility Testing

Antibiotic susceptibility profiling of all isolates was achieved by the Kirby–Bauer disk diffusion technique. Inoculums equivalent to the opacity of 0.5 McFarland standards was prepared and swabbed over the MHA surface; exposed to antibiotic disks, and then incubated face up at 37°C for 24 hours. The diameter of zones of inhibition was measured and categorized as sensitive, intermediate, and resistant according to the table described in CLSI (2022). The Standard antimicrobial disks (oxoid, UK) used were Penicillin (10 mg), Ciprofloxacin (5 mg), Clindamycin (2 mg), Gentamicin (10 mg), Erythromycin (15 mg), Chloramphenicol (30 mg), Ampicillin (10 mg), Tetracycline (30mg) and Trimethoprim-sulfamethoxazole (25 mg) and Cefoxitin (30 mg) (Humphries et al., 2021).

Testing for MRSA

MRSA was detected by placing 30µg of Cefoxitin per disk on Mueller-Hinton agar. The zone of inhibition was determined after 24 hours of incubation at 35⁰ C. All isolates ≤ 24 mm of cefoxitin, were considered as MRSA (CLSI, 2020).

Variables

Prevalence of MRSA nasal carriage was dependent variable. While, Variable like age, sex, department, year of study, Presence or history of having an indwelling medical device, previous hospitalization in the past year, cigarette smoking, washing hands upon arriving at the hospital, washing hands after every patient contact, hand washing before and after meal, alcohol use, frequency of hand washing with soap, use of gloves while handling patients, nose picking habit, sharing of clothing, number of students in the dormitory, mean exposure to hospital, history of chronic disease, ways of antibiotic usage, participate in invasive procedures were independent variables.

Data and Laboratory Quality Control

Staphylococcus aureus ATCC 25923 and Escherichia coli (ATCC 25922) was used for a positive and negative control for laboratory investigations. All culture media were prepared by following the manufacturer’s instructions, and sterility was checked by incubating 5% of each batch of the prepared culture media at 37°C overnight. All culture plates and antibiotic discs were stored at the recommended refrigeration temperature (2-8^oC). The questionnaire was pretested on Health Science students with Clinical attachment at Oda Bultum University, moreover, the completeness of each data was assured and also any double entry of data was checked. The training was given to both data collectors and supervisors.

Data analysis

The data was entered and analyzed by SPSS version 25 software. Descriptive statistical analysis was used to summarize the findings. Chi-square test was used to assess difference between dependent and independent variables. Variables with a p-value < 0.05 were considered statistically significant.

Socio-demographic characteristics

A total of 250 students with clinical attachment were involved in this study. The majority of the students were male 158 (63.2%). Ages ranged from 19 to 29 years (mean 20.6, standard deviation (SD) ± 2.2 years). Among the participants, 121 (48.4%) were Medical students and 83(33.2%) were 4th -year students.

Behavioral-related characteristics

In the present study, 228 (91.2) were nonsmokers 158 (63.2%) washed their hands upon arriving at the hospital, 160(64.0%) washed their hands after every contact with patients, 244 (97.6%) washed their hands before and after meals, 220(88%) of them washed their hands while leaving the hospital. from the study participants, 158 (63.2%) did not consume alcohol, 180(72.0%) washed their hands with soap frequently, 142(56.2%) had a habit of using gloves while handling patients, 158(63.2%) had nose picking habit,180 (72.0%) had a habit of sharing of cloth and 148(59.2%) had more than 4 students in their dormitory.

Clinical related characteristics

In this study, 101(40.4%), 77(30.8%), 61(24.4%), 24 (9.6%), and 40(16.0%) of the students had greater than 2 years of mean exposure to hospital, participated in invasive procedures, history of admission to ICU, history of having indwelling medical devices, history of previous hospitalization in the past 1 year, 7(2.8%) had chronic diseases. While 152(60.8%) used a full course of antibiotics (Table 2)

Table 1

Socio-demographic characteristics of nasal carriage rate of *Staphylococcus aureus* among students of HUCHMS with clinical attachment, Harar Eastern Ethiopia, 2022
Variable		Number	Percent (%)
Gender	Male	158	63.2
Gender	Female	92	36.8
Age	< 22	88	35.2
Age	>=22	162	64.8
Department	Medical	121	48.4
	Midwifery	25	10.0
	MLS	18	7.2
	Nursing	31	12.4
	Paediatrics	18	7.2
	Pharmacy	10	4.0
	Psychiatry	17	6.8
	Public health	10	4.0
Year of Study	2nd	43	17.2
	3rd	33	13.2
	4th	83	33.2
	5th	51	20.4
	6th	40	16.0

Table 2

Clinical characteristics of nasal carriage rate of *Staphylococcus aureus* among students of HUCHMS with clinical attachment, Harar Eastern Ethiopia, 2022
Variable		Number	Percent (%)
Mean exposure to hospital	Less than 6 months	149	59.6
Mean exposure to hospital	Greater than 2 years	101	40.4
Admitted to ICU	Yes	61	24.4
Admitted to ICU	No	189	75.6
Presence or history of having an indwelling medical device	Yes	24	9.6
Presence or history of having an indwelling medical device	No	226	90.4
Previous hospitalization in the past year	Yes	40	16.0
Previous hospitalization in the past year	No	210	84
History of chronic disease	Yes	7	2.8
History of chronic disease	No	243	97.2
Ways of antibiotic usage	Full course	152	60.8
Ways of antibiotic usage	Incomplete course	98	39.2
Participate in an invasive procedure	Yes	77	30.8
Participate in an invasive procedure	No	173	69.2

Prevalence of S. aureus and MRSA

The prevalence of S. aureus and MRSA in this study were found to be 8% (20/250, 95% CI: 4.6%, 11.3%) and 4.8% (12/250, 95% CI: 2.1%, 7.4%) respectively.

Associated factors

The study showed, among several contributing factors only nose picking habit (P = 0.001) and number of students in the dormitory (P = 0.05) showed a statistically significant association with nasal carriage rate of MRSA (Table 3).

Table 3

Association of socio-demographic, behavioural and clinical characteristics of nasal carriage rate of *Staphylococcus aureus* among students of HUCHMS with clinical attachment, Harar Eastern Ethiopia (n = 20).
Variables	Categories		MRSA			Chi-square result	P-value
		Positive (%)		Negative (%)
Gender	Male	8 (3.2%)		150 (60%)		0.046	.830
	Female	4 (1.6%)		88 (35.2%)
Age	< 22 years	7 (2.8%)		81 (32.4%)		1.00	0.317
	>=22 years	5 (2%)		157 (62.8%)
Department	Medical	4 (1.6%)		117(46.8%)		3.41	.844
	Midwifery	1 (0.4%)		24 (9.6%)
	MLS	1(0.4%)		17 (6.8%)
	Nursing	6 (2.4%)			25 (10%)
Year of Study	2nd	1(0.4%)			42(16.8%)	4.316	.365
	3rd	2(0.8%)			31(12.8%)
	4th	6(2.4%)			77(30.8%)
	5th	3(1.2%)			48(19.2%)
Cigarette smoking	Yes	2(0.8%)			20(8%)	1.005	.316
	No	10(4%)			218 (87.2%)
Washing hands upon arriving at the hospital	Yes	7(2.8%)			151(60.4%)	0.207	0.649
	No	5(2%)			87(34.8%)
Washing hands after every patient contact	Yes	4(1.6%)			156(63.04%)	0.072	.788
	No	8(3.2%)			82(32.8%)
Hand washing before and after meal	Yes	10(4%)			234(93.6%)	0.256	.613
	No	2(0.8%)			4(1.6%)
Hand washing before and after meal	Yes	9(3.6%)			211(84.4%)	0.039	.843
	No	3(1.2%)			27(10.8%)
Alcohol use	Always	2(0.8%)			8(3.2%)	0.598	0.741
	Sometimes	4(1.6%)			78(31.2%)
	No	6(2.4%)			152(60.8%)
Frequency of hand washing with soap	Frequently	5(2%)			175(70%)	3.21	.200
	Occasionally	5(2%)			60(24%)
Use of gloves while handling patients	Always	5(2%)			137(54.8%)	1.094	.579
	Sometimes	5(2%)			89(35.6%)
	Rarely	2(0.8% )			12(4.8%)
Nose picking habit	Yes	8(3.2%)			30(12%)	16.7	.001
	No	4(1.6%)			208(83.2%)
Sharing of clothing	Yes	6(2.4%)			64(25.6%)	0.744	.388
	No	6(2.4%)			174(69.6%)
Number of students in the dormitory	< 4	3(1.6%)			133(36.8%)	3.6	.05
	> 4	9(3.2%)			105(56%)
Mean exposure to hospital	< 2 years	7 (2.8%)			142(56.8%)	3.662	.300
	> 2 years	5(2%)			96(38.4%)
Admitted to ICU	Yes	3(0.4%)			58(24%)	1.171	.279
	No	9(3.6%)			180(72%)
Presence or history of having indwelling medical devices	Yes	3(1.2%)			21(8.4%)	0.002	.965
	No	9(3.6%)			217(86.8%)
Previous hospitalization in the past 1 year	Yes	5(2%)			35(14%)	1.519	.218
	No	7(2.8%)			203(81.2%)
History of chronic disease	Yes	2(0.8%)			5(2%)	1.984	.159
	No	10(4%)			233(93.2%)
Ways of antibiotic usage	Full course	4(1.6%)			148(59.2%)	1.891	.169
	Incomplete course	8(3.2%)			90(36%)
Participate in invasive procedures	Yes	8(3.2%)			69(27.6%)	2.114	.146
	No	4(1.6%)			159(63.6%)

Antibiotic Susceptibility Pattern MRSA

In this finding, MRSA strains exhibited a stark resistance profile against several antibiotics. Notably, 100% resistance rates were observed against Ampicillin and Penicillin. Tetracycline had resistance rates of 66.7%, Erythromycin 25%, Ciprofloxacin 25%, Co-trimoxazole 16%, and Gentamicin 16% of cases. Conversely, Chloramphenicol and Clyndamycin were fully susceptible in all cases.

In the present study, the prevalence of S.aureus among students of HUCHMS was 8% (20/250, 95% CI: 4.6%, 11.3%). Bhatta et al. (2018) reported a prevalence of 35% among medical students at Manipal College in Nepal, which is significantly higher than the 8% prevalence observed in the present study. Similarly, Zakai (2015) found a prevalence of 25.3% among medical students at King Abdul Aziz University in Saudi Arabia, and Mekuriya et al. (2022) reported a prevalence of 27.1% among students at Arbaminch University in Ethiopia, both of which are considerably higher than the prevalence observed in the present study. These differences could be due to due to variation in Variations in sample size and sampling strategy. in addition, the carriage rate might be influenced by Variations in study populations, including demographics, geographical locations, and environmental factors, which could contribute to differences in prevalence rates.

The prevalence of MRSA in this study was found to be 4.8% (95% CI: 2.1%, 7.4%). Comparing this finding to previous studies, it aligns closely with the MRSA prevalence reported in a study where 5.19% of the isolates were identified as MRSA. However, it is notably higher than the reported rates in Jordan (2.8%) and Saudi Arabia (3.3%). Conversely, it is substantially lower than the MRSA prevalence reported in Nigeria (61.8%) and Malaysia (13.9%). Further research, including larger-scale epidemiological studies and comparative analyses, may help elucidate the underlying factors driving differences in MRSA prevalence among student populations in diverse geographical regions.

The total prevalence of MRSA in this study was 4.8% (95% CI: 2.1%, 7.4%). This finding is higher than, 2.8% of Jordan (Alzoubi et al., 2020) 3.3% in Saudi (Albusayes et al., 2019), less than 61.8%, Nigeria (Alli et al., 2022), 13.9% Malaysia (Anbazhagan et al.).

In current study, the habit of nose picking and living in a dormitory environment with more than four students, Like (Mekuriya et al., 2022b) but Unlike (Abdelmalek et al., 2022), were found to be potential contributing factors to MRSA nasal carriage. This is due to the fact that nose picking can introduce bacteria from the nasal mucosa into the hands, which may subsequently contaminate surfaces and contribute to the spread of MRSA. Similarly, Dormitories often entail communal living arrangements, where close quarters and shared facilities increase the likelihood of MRSA transmission. Factors such as limited personal space and frequent social interactions provide ample opportunities for MRSA to spread among residents.

The findings regarding antibiotic resistance patterns in the MRSA isolates also present important insights into the susceptibility and resistance levels to commonly used antibiotics. The data indicates a concerning 100% resistance rate to both Ampicillin and Penicillin, which are commonly prescribed antibiotics. This highlights a critical issue in the region concerning the effectiveness of these medications against MRSA.

The resistance rates for other antibiotics such as Tetracycline, Erythromycin, Ciprofloxacin, and Co-trimoxazole show varying degrees of resistance ranging from 16% to 66.7%. This variability suggests that different antibiotics may still be effective against certain strains of bacteria while others exhibit higher levels of resistance.

A study conducted at Jimma University (Efa et al., 2019b) observed the similar resistance rates to Erythromycin and Tetracycline to our study. whereas, another study at Arba Minch University reported similar resistance rates for Tetracycline, Ampicillin and Penicillin but lower resistance to Ciprofloxacin compared to the current findings (Mekuriya et al., 2022c). These discrepancies underscore the dynamic nature of MRSA resistance and the influence of regional variations, antibiotic usage patterns, and genetic factors.

In our findings, a resistance rate of 16% was observed for both Co-trimoxazole and Gentamicin. Interestingly, while the resistance to Co-trimoxazole remains consistent with previous findings from a study conducted at Jimma (Efa et al., 2019b), the resistance to Gentamicin appears to be higher in this study. This difference in resistance levels may stem from factors like genetic mutations or horizontal gene transfer among bacteria. Discrepancies in the accessibility and utilization of alternative antibiotics can impose selective pressure on bacterial communities, resulting in fluctuations in resistance patterns to specific antibiotics over time.

Notably, Chloramphenicol and Clindamycin displayed full susceptibility across all cases tested; indicating their efficacy in treating the MRSA isolates under study and this is in contrast to the results of other works reported by (Kitti et al., 2011) and (Neela et al., 2008). This information is crucial when selecting appropriate antibiotic treatments to ensure effective patient care and combat the challenge of antibiotic resistance. Unlike the study where all MRSA isolates were resistant to clindamycin, in this study Clindamycin displayed full susceptibility across all cases tested.

The study reveals significant prevalence of MRSA and high antibiotic resistance rates. Nasal carriage of MRSA is significantly associated with nose-picking habit and dormitory occupancy. Effective infection control measures, emphasizing hand hygiene and reducing environmental transmission, are crucial. Clinicians should be vigilant in prescribing antibiotics, considering local resistance patterns. Public health campaigns targeting high-risk behaviors and communal living environments may help mitigate MRSA spread.

Ethical approval and consent

Ethical clearance for the study was obtained from the Institutional Health Research Ethics Review Committee (IHRERC) of Haramaya University College of Health and Medical Science. Informed written consent was obtained from each participant after explaining the objectives of the study. Information obtained from study participants was kept confidential. The participants were informed about positive for MRSA.

Consent for publication

Not applicable.

Availability of data and materials

The data sets generated during and/or analyzed during the current study are available from the corresponding authors on reasonable request.

Conflict of interest

The author declares no conflict of interest.

Funding statement

No funding

Acknowledgements

We are thankful to division of Medical Microbiology staff for their unreserved support. We gratefully thank HFSUH students and administrative for their kind corporation.

Authors’ contribution

All authors made a significant contribution to the work reported, whether that is in the conception, study design, execution, acquisition of data, analysis, and interpretation, or in all these areas; took part in drafting, revising or critically reviewing the article; gave final approval of the version to be published; have agreed on the journal to which the article has been submitted; and agree to be accountable for all aspects of the work.

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No competing interests reported.

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Nasal Carriage Rate Of Staphylococcus aureus, Associated Factor And Its Antibiotic Susceptibility Patterns Among Students Of Collage Of Health And Medical Science WITH Clinical Attachment

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Abstract

Figures

Introduction

Methods and Materials

Study Area and Period

Study Design, Period and Population

Eligibility Criteria

Sample size determination and sampling technique

Data Collection Instruments and Procedures

Specimen collection and Transportation

Laboratory Isolation and Identification

Antimicrobial Susceptibility Testing

Testing for MRSA

Variables

Data and Laboratory Quality Control

Data analysis

Results

Socio-demographic characteristics

Behavioral-related characteristics

Clinical related characteristics

Associated factors

Antibiotic Susceptibility Pattern MRSA

Discussion

Conclusion and Recommendation

Declarations

References

Additional Declarations

Supplementary Files

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