antibiotic resistance profiles of staphylococcus aureus

Frontiers of Knowledge Journal Series | International Journal of Medical and Biosciences | ISSN: 2635-3628 | Vol. 2 Issue 2 (June, 2019)

Open Access Journal www.smrpi.com 1

Antibiotic Resistance Profiles of Staphylococcus aureus Isolated from

Fomites in Community Schools within Abeokuta Environs Leading to

Detection of MRSA. Akinrotoye, K. P.1 Bankole, M.O. 2 Akinduti, P.A.3 Lanlokun, O.A.4

Department of Microbiology, College of Biosciences, Federal University of Agriculture, P.M.B

2240,110001, Abeokuta, Ogun State, (Nigeria)

Department of Microbiology, College of Biosciences, Federal University of

Agriculture, P.M.B 2240,110001, Abeokuta, Ogun State,

(Nigeria)

Department Biological Sciences, College of Science and

Technology, Covenant University, Ota, Ogun State,

(Nigeria)

Department of Microbiology, College of Biosciences, Federal University of

Agriculture, P.M.B 2240,110001, Abeokuta, Ogun State,

(Nigeria)

Abstract

MRSA is known to show resistance to β-lactam class of antibiotics and is among the highest

superbugs posing dangerous threats to humans which cause serious infectious diseases, with

extended resistance to other antibiotics making treatment ineffective. An additional

challenging feature of MRSA bacteria is its rapid dissemination to human and animal

through different fomites. This study aimed at determining the prevalence and antimicrobial

susceptibility pattern of MRSA isolated from toilets, offices and classroom door handles in

community schools within Abeokuta; which might serve as a reservoir for dissemination to

the general population of students and staffs within the school community. Fifteen community

schools in Abeokuta environs were picked for sampling, in which 300 sample swabs were

taken from the toilet; office and classroom door handles using sterile swabs stick moistened

with buffered peptone water. Growth and Isolation of S. aureus were carried out using

Mannitol salt agar, while antimicrobial susceptibility test was performed on the isolates to

determine resistance profile to available antibiotics used while Multiple Antibiotic Resistance

index (MARI) of MRSA was determined in addition to their haemolytic pattern on blood agar.

The occurrence rate of Staphylococcus spp isolated from fomites is 50.60 %, while the

prevalence rate of MRSA is 2.99 % as determined by antimicrobial susceptibility test. High

Multiple Antibiotics Resistance index greater than 0.4 was observed in all MRSA isolates

while 3 out of nine isolates showed partial α-haemolytic reaction representing 40 % and the

remaining 6 representing 60 % showed γ- haemolytic reaction. The detection of MRSA in this

study emphasizes the need to set up surveillance programs to monitor the spread of MRSA

and formulate preventive measures to prevent the spread of MRSA amongst students and

staffs hence curbing its dissemination.

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Keywords: MRSA, Community Schools, Antimicrobial susceptibility, fomites, Public Health,

MARI

1. BACKGROUND OF THE STUDY

Staphylococcus aureus is a bacterium which is commonly found as commensals on part of

the human body of healthy individuals (Plata et al., 2009). Methicillin-Resistant

Staphylococcus aureus- with an acronym MRSA is S. aureus that is resistance to the beta (β)-

lactam class of antibiotics. According to the Centres for Disease Control and Prevention

(CDC, 2013), MRSA is among the among the highest superbugs posing dangerous threats to

humans of antibiotic resistant pathogens; although MRSA causes serious infectious diseases,

many antibiotics remain resistance to it hence making treatment ineffective.

As the numbers of severe invasive MRSA infections acquired in health-care settings continue

to decline, the numbers of such infections caused by pathogenic bacteria of medical

importance among the general public continue to rise and are transmitted through different

contacts (fomites) within our community i.e. schools (Dirk, 2006; Akinrotoye et al., 2018).

Historically, S. aureus rapidly developed resistance to antibiotics as they were brought

successively into clinical use, and doctors came to recognize resistance to each such new

drug within months to years of its introduction. The first penicillin resistant S. aureus

pathogens emerged by 1942 after its introduction in 1940, Staphylococcus aureus remains

resistant to that original type of penicillin and to other members of this class of antibiotics till

date (Otto, 2012).

S. aureus becomes MRSA after acquiring genes that encode resistance to the broader class of

β-lactam antibiotics. The specific gene taken up by S. aureus to make it resistant to

Methicillin is called mecA. This gene is carried together with a larger set of genes, known as

SCCmec (Staphylococcal cassette chromosome), that is mobile and capable of inserting into

the DNA of other S. aureus bacteria. MRSA strains can also carry resistance to antibiotics

other than members of the b-lactam class. This multidrug resistance makes the infections

caused by these S. aureus strains very difficult to treat. In addition to producing toxins and

virulence factors, MRSA bacteria can generate biofilms, sticky layers and clumps of cells that

enable bacteria within them to adhere to medical devices such as catheters and implants.




A biofilm protects the bacteria within it from the actions of antibiotics and of the human

immune system (Otto, 2012). The protective strategies used by MRSA strains to evade the

host immune system in combination with multidrug resistance all contribute to the virulence

of MRSA. Patients with these infections can have high morbidity and mortality rates, and

caring for them contributes to high health-care costs for these patients (due to treatment

difficulties and longer hospital stays).

An additional challenging feature of MRSA bacteria is their hardiness. They can survive for

prolonged periods on surfaces and objects such as sinks, toilets, door handles, floors, medical

devices, bed linens, cleaning equipment, and clothing. Therefore, extensive contact control

and disinfection procedures are needed to limit the spread of MRSA in health-care and other

community settings e.g. community school, stadia, markets, Malls etc.

MRSA can be divided into 3 categories:

• Healthcare-associated (HA)-MRSA bacteria contracted in health-care settings

• Community-associated (CA)-MRSA bacteria contracted outside of health-care-related

environments (more common in close-knit communities) e.g. public schools

• Livestock-associated (LA)-MRSA – MRSA in a livestock (most commonly pigs) reservoir

transmitted from animals to infect people working with or in close contact with those

animals. Animals can acquire both HA-MRSA and CA-MRSA strains (Smith et al., 2013).

This study aims to determine and know if MRSA is present and detected from swabs sample

taken from fomites in the community schools within Abeokuta environs, occurrence and

prevalence rate of MRSA in all of the randomly selected community schools. Probable

occurrence of MRSA in various centre of learning within Abeokuta may pose a threat to the

health of students and staffs in the community school, which might serve as a possible

reservoir of MRSA (point of contact) to the general population within the community.

2. MATERIALS AND METHODS

Study site: Study site was Abeokuta environs. Abeokuta has three LGAs namely; Odeda

Local Government Area, Abeokuta South Local Government and Abeokuta North Local

Government Area. Arc GIS 9.3 software was used to display the map of the study areas and

study site. GPS was used to georeference the study sites namely Abeokuta South LGA,

Abeokuta North LGA and Odeda LGA, Arc GIS 9.3 software was used to display the map of

the study sites using their GPS coordinates.




Plate I: Geographical coordinates of the study site collected through Arc GIS 9.3

software.

2.1 Study population: The population of interest included selected community/public

secondary schools in Abeokuta, Nigeria. The Principal of the schools gave consent of their

willingness to participate in the study.




Sample Size: (n) = Z2 * (p) * (1-p) /c 2 (Maccallum et al., 2001)

• Z = 1.96 (95 %)

• p = Occurrence rate of 20.23% (0.2023) of MRSA among environmental

samples from previous studies

• c = Confidence interval, 0.05. The minimum number of 296 environmental

samples was calculated.

Cross-sectional study design: This was prepared by randomization in which the

community/public schools of interest was picked randomly and sampled across Abeokuta

environs.

2.2. Approval from Principals

The schools contacted was selected from a list of community/public schools in Abeokuta

environs, Ogun State; Nigeria. The Principals of the various community schools were brief

and were asked for voluntary participation; principals of the various community schools gave

approval by signing a consent form given to them.

2.3 Collection of sample swabs from fomites

300 swab samples were taken from various door handles (fomites) such as class rooms,

offices, staff toilets, student toilets in selected public community schools in Abeokuta,

Nigeria. Fomite was swabbed with a swab stick moistened with buffered peptone water and

kept at room temperature by placing them in an ice-pack cooler. The swab samples were

labelled to aid identification and then transported to the Laboratory for further examination

and culture.

2.4 Culture and examination of sample swabs

The sample swabs was shaken vigorously so as to displace the microorganisms into the

buffered peptone water solution, after which it was plated into Mannitol salt agar media and

plates incubated at 35°C for 24 h. The high concentration of sodium chloride in selective

media of Mannitol salt agar does not allow the growth of any other bacteria species on the

agar media except that of Staphylococcus species, which is indicated by a change in the

colour of red-phenol to a golden or yellowish coloration (Collee et al., 1996). It was later

sub-cultured on blood agar to determine their haemolysis parameter.




2.4.1 Biochemical Characterization of bacterial isolates

Bacteria isolated from the various fomites were morphologically examined to determine the

shape, size, elevation, surface, margin, colour, odour, and pigmentation of the various

colonies on the agar plate; Biochemical tests including catalase, coagulase, oxidase, citrate

utilization, Voges-Proskaeur, and methyl-red were also carried out on the isolates (Fawole

and Oso, 1998; Cheesbrough, 2006) for further identification and compared with Bergeys

Manual of Determinative Bacteriology. Coagulase test and Novobiocin was used to

differentiate between Staphylococcus aureus and S. saprophyticus.

2.5 Testing for antimicrobial susceptibility pattern

Antibiotics acquired for the antimicrobial susceptibility test for the S. aureus include

gentamicin (10 ug), Trimethoprim + sulfamethoxadole (30 μg), ofloxacin (5 μg), pefloxacin

(10 μg), cotrimoxazole (25 μg), chloramphenicol (5 μg), ciprofloxacin (5 μg), erythromycin

(5 μg), amoxycillin (10 μg), oxacillin (5 μg). 10 μL of 0.5 McFarland standards (106 CFU/ml)

of Staphylococcus aureus were inoculated and plated on Mueller Hinton agar plates after

which the antibiotics was placed at different region of the agar plate with the aid of a forceps

and incubated at 37o C for 24 h.

The agar plate was then observed for clearer zone around the disc, which is then determined

with rule-meter calibrated in mm. Oxacillin disc (5 μg) was improvised and used to test for

oxacillin resistance in Staphylococcus aureus isolated from various fomites, a diameter of

zone ≤ 10 mm will be regarded as Methicillin resistance (CLSI, 2011; Deresinski, 2005) and

later confirmed according to the National Committee for Clinical Laboratory Standard.

2.5.1 Multiple Antibiotic Resistance (MAR) Index Determination

The Multiple Antibiotic Resistances (MAR) Index was calculated for each isolate as shown in

the equation below. MAR index is the number of antibiotic(s) to which the organism is

resistant divided by the total number of antibiotics tested (Akinjogunla and Enabulele, 2010)

MARI = Number of Antibiotic (s) to which isolate was resistant

Total number of antibiotics tested

2.5.2 Pilot Study/ Feasibility Study

A control reference Methicillin Resistant Staphylococcus aureus (ATCC 33591) was

acquired to conduct the pilot study which was used as the control for all other parameters.




2.6 Statistical Analysis

Data collected and gathered were analysed using Microsoft Excel (Windows 10).

2.7 Ethical approval

Ethical clearance for the study was obtained from both State Ministry for Health &

Education; Ogun State and was cleared by the Ethical Review Committee from College of

Biosciences (COLBIOS), FUNAAB.

3. RESULTS AND DISCUSSION

3.1 Sample Collection

Figure 1 shows a total of 300 swabs collected from fomites in randomly selected secondary

schools in the three Abeokuta Local government areas which were distributed as follows:

Abeokuta South LGA- office doors (27), classroom doors (33), toilet doors (23), toilet water

closet handle (17), Abeokuta North LGA- office doors (27), classroom doors (39), Toilet

doors (21), Toilet WC handle (15); Odeda LGA- office doors (28), classroom doors (35),

Toilet (21), Toilet WC handle (16). Highest number of swabs was obtained from the class

room doors and lowest number of swabs from the toilet doors respectively from all the local

government areas.

TOILET DOORS

OFFICE DOORS

CLASSROOM DOORS

TOILET WC HANDLE




Figure 1: Comparative level of swab samples collection in various schools in Abeokuta South, Abeokuta North and Odeda Local government, areas of Abeokuta.

3.2 Prevalence of Staphylococci organisms

A total of 300 sample swabs collected from fomites in different community secondary

schools were microbiologically evaluated and processed. 83 Staphylococcal organisms were

isolated from these fomites comprising 3 species namely, Staphylococcus aureus (50.60 %),

Staphylococcus saprophyticus (20.48 %) and Micrococcus spp (28.92 %).

Plate II: Growth of Staphylococcus aureus on Mannitol Salt agar




Figure 2: Percentage Distribution of Staphylococcal species in all sample swabs from the three Local Government Areas in Abeokuta Environs

3.2.1 Antibiotic susceptibility test for S. aureus isolates from fomites

Antibiotic susceptibility test were carried out on all the 42 S. aureus isolated from the fomites

which show the proportion of S.aureus isolates which are considered to be susceptible,

intermediate or resistant to the various antibiotics as shown in Fig 3. All S. aureus tested were

highly resistant to ampicillin (100 %), Streptomycin (100 %), Amoxicillin (100 %), but

showed various level of resistance to Trimethoprim/Sulfamethoxazole (77.78 %),

Cotrimoxazole (66.67 %), Erythromycin (33.33 %), oxacillin (21.43 %) and

Chloramphenicol (44.44 %).




Plate III: Multi drug resistance in S.aureus isolated from fomites within school in Abeokuta

Figure 3: Antimicrobial susceptibility profile of Staphylococcus aureus isolates from fomites in selected secondary schools in Abeokuta Environs

3.2.2 MAR Index of MRSA isolate

Table 1 shows the Multiple Antibiotic Resistance (MAR) index of the nine (9) MRSA strains in

which second isolate has the maximum MAR index of 0.8, followed by the third, fifth and

ninth isolates with MAR index of 0.7. The sixth and seventh isolates have the lowest MAR

index of 0.44 and 0.55 respectively.

sensitive

intermediate

resistant




Table 1: MAR Index of MRSA isolates Isolate Resistance pattern MAR Index 1 GEN, COT, AMX, TSX, OXL, EMX 0.6 2 GEN,COT,OFL, AMX, CPX, OXL, TSX, PFX 0.8 3 GEN, COT, AMX, TSX, CMP, EMX, OXL 0.7 4 GEN, AMX, PFX, CMP, CPX, OXL 0.6 5 GEN, OFL, AMX, TSX, OXL, CMP 0.6 6 GEN, COT, AMX, OXL 0.44 7 COT, AMX, EMX, TSX, OXL 0.55 8 AMX, TSX, CMP, OFL, OXL, PFX 0.67 9 AMX, EMX, TSX, OFL, COT, OXL 0.67 KEY: GEN= GENTAMYCIN, COT= COTRIMOXAZOLE, OFL= OFLOXACIN, AMX= AMOXYCILLIN, CPX= CIPROFLOXACIN, CMP= CHLORAMPHENICOL, EMX= ERYTHROMYCIN, TSX= TRIMETHOPRIM+SULFAMETHOXADOLE, PFX= PEFLOXACIN, OXL= OXACILLIN, MAR=MULTIPLE ANTIBIOTIC RESISTANCE

3.3 MRSA growth on blood agar

Plate IV: Growth of MRSA on blood agar showing α-haemolysis and γ-haemolysis




Staphylococcus aureus were isolated from fomites such as classroom, office, toilet and toilet

water closet door handles in selected secondary schools within Abeokuta environs (Abeokuta

North LGA, Abeokuta South LGA and Odeda LGA). Methicillin Resistance Staphylococcus

aureus (MRSA) is the leading cause of bacterial infections, causing a wide range of diseases

such as bacteraemia, wound infection, septicaemia and pneumonia; but when it has not acquired

the resistant gene (just the normal S.aureus), it is an important human friendly microorganisms

which is often found as commensal on body surface but its transfer to other part of the human

body may lead to a wide variety of infections (David and Daum, 2010). From this study, some

strains of S. aureus isolated from the fomites were found to be resistant to oxacillin confirming

them to be Methicillin Resistant S. aureus (Taiwo et al., 2004) which is of a major concern to the

public health safety of the students and staffs within the community (secondary schools) in

Abeokuta environs.

According to the antimicrobial susceptibility test, using the disk diffusion method; strains of S.

aureus isolated shows high resistance to ampicillin (100%), Streptomycin (100%), Amoxicillin

(100%), but moderate resistance to Trimethoprim (77.78%), Cotrimoxazole (66.67%), but low

resistance to Erythromycin (33.33%), oxacillin (21.43 %) and Chloramphenicol (44.44%).

Based on this resistance profile, S. aureus was shown to be Multi-drug resistant and the clinical

importance of this is that these drugs should not constitute a first line of therapeutic treatment in

any hospital setting around the environs (Albuquerque et al., 2007).

The high level of resistance to the β-lactam antibiotics (Amoxicillin and ampicillin) in this study

confirm β-lactamase activity which was due to the presence of mecA gene which encodes a

modified Penicillin-binding protein which has low affinity for β-lactams (Hartman and Tomasz,

1984; Katayama et al., 2000; Li et al., 2011; Garci et al., 2011). The antimicrobial resistance

profile also revealed that the levels of resistance to trimethoprim/sulfamethoxazole, ofloxacin,

ciprofloxacin were remarkable among the S. aureus strains which support earlier report by

(Fridkin et al., 2005; Nordmann and Naas, 2005; Polyzou et al., 2001). Since our study was

cross-sectional, data on contacts between staffs and students were not collected limiting the

investigation on possible transfer of MRSA from one sub-group to another within the school

community.




A Prevalence of 50.60 % for S. aureus was recorded in this cross sectional study in which 42

isolates of S. aureus were confirmed; 2.99 % (9 isolates) were confirmed to be MRSA by both

antimicrobial susceptibility test and PCR amplification. The prevalence rate recorded for MRSA

in this study were much lower than one recorded for MRSA in a similar study carried out in

Nairobi county, Kenya (Caroline et al., 2013) in which a prevalence rate of 15 % was found. The

results obtained from this study indicate that the prevalence rate of MRSA varies from one

geographical region to another, since it is clear that MRSA is a threat to the health of both

students and staffs within the school community; it is therefore pertinent to put in place infection

control measures which may be necessary to nip its rapid dissemination amongst the population

(Ghebremedhin et al., 2009; Okon et al., 2011, Akinrotoye et al., 2018).

Lack of surveillance programs in Nigeria monitoring the prevalence of MRSA (Taiwo et al.,

2004; WHO, 2014) in school community serves as hindrance to conclusive evidence whether

there has been an increase or decrease in the prevalence rate of MRSA in the school community

within Abeokuta environs.

4. SUMMARY AND CONCLUSION

4.1 Summary

This study has described the Antibiotic resistance profiles and Multiple Antibiotics Resistance

Index (MAR) of MRSA strains obtained from schools within Abeokuta environs of Ogun State.

This information is helpful in establishing effective infection control measures in health care

settings and school in Ogun State, Nigeria. Methicillin Resistant S. aureus are present on fomites

from selected secondary schools within Abeokuta environs hence preventive measures should be

formulated in order to regularly curb its dissemination and monitor the spread of MRSA and

other bacteria of public health importance.

4.2 Conclusion

Hygiene measures such as hand washing should be encouraged in schools across Abeokuta and

other part of the country to prevent the spread of Staphylococcus aureus amongst students and

staffs which is capable of developing resistance to various antibiotics.




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Authors

1 Akinrotoye Kehinde Peter (B.Tech, MSc)

He has been carrying out research in the area of

diarrhoeagenic bacteria, fermented Palm wine as alternatives

to antibiotics, Methicillin Resistant Bacteria and Public

Health at Federal University of Technology, Akure and

Federal University of Agriculture, Abeokuta for some years

now. He has a Bachelor of Technology (B. Tech) degree in

Microbiology obtained from FUTA and a Master of Science (MSc) in Medical

Microbiology & Public Health from Federal University of Agriculture, Abeokuta.

He has membership affiliation to America Society for Microbiology (ASM), Society

for Applied Microbiology (Sfam), RANEXT, NSM etc.

2 Prof. (Mrs.) Mobolaji Olufunmilayo BANKOLE (B.Sc., M.Sc., Ph.D.)

She instructed different Microbiology related courses in

Federal University of Agriculture, Abeokuta at various

levels from Part-time, Degree and Post-graduate level. She

had her Bachelor of Science Degree, Masters and PhD

from ABU, Zaria. She is currently a retired staff of the

Federal University of Agriculture, Abeokuta in the

Department of Microbiology. Her research is focused on Food Microbiology, Public

Health, Food Safety and Enzymes; she has won several travel grants and research

grants.

3 Dr. P.A. Akinduti (B.sc, MSc, Ph.D.) He is currently a Lecturer of Covenant University, Ota in

the Department of Biological Sciences. His research

focuses on Antimicrobial Resistance, MDR, Genomic

Analysis, MRSA etc. A recipient of several researches

grants; also has membership affiliation to various local

and international scientific organizations.




4 Lanlokun Olabisi (BSc, MSc)

She is currently pursuing her Doctorate degree in Food

Microbiology from the same university (Federal

University of Agriculture, Abeokuta) where she bags her

degree and Masters. Her research interest spans from

Mycotoxins, Heavy Metal contamination in staple foods

and food spoilage.


antibiotic resistance profiles of staphylococcus aureus

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