|Year : 2018 | Volume
| Issue : 1 | Page : 6-10
Methicillin-Resistant Staphylococcus aureus in a Central Nigeria Tertiary Hospital
Nasiru Abdullahi, Kenneth Chukwuemeka Iregbu
Department of Medical Microbiology and Parasitology, National Hospital, Abuja, Nigeria
|Date of Web Publication||11-Jun-2018|
Dr. Nasiru Abdullahi
Department of Medical Microbiology and Parasitology, National Hospital, Abuja, PMB 425 Garki, Abuja 900 001
Source of Support: None, Conflict of Interest: None
Background: Methicillin-resistant Staphylococcus aureus (MRSA) is a significant cause of both health care- and community- associated infections worldwide and do present therapeutic challenges to beta-lactam antibiotics and other antibiotics due to the development of multidrug resistance. Aim: This study was carried out to determine the prevalence and antibiotic susceptibility profile of MRSA among patients at National Hospital Abuja with a view to providing information that will guide rational choice of antimicrobial agents in the empirical therapy of its infections. Materials and Methods: Between April 2014 and August 2015, clinical samples of patients submitted to Medical Microbiology laboratory of the hospital were processed and all Staphylococcus aureus isolates recovered, using standard laboratory methods. They were subjected to antibiotic susceptibility testing using the modified Kirby Bauer disc diffusion technique with zones of inhibition interpreted according to the Clinical and Laboratory Standard Institute (CLSI) guidelines. Methicillin resistance was determined using cefoxitin disc diffusion. Other clinical data of the patients were gathered along for analysis. Results: Of the 360 S. aureus isolates recovered, 97 (26.9%) were MRSA. All (100%) the MRSA isolates were susceptible to vancomycin, 88 (90.7%) to imipenem and 71 (73.2%) to clindamycin. All (100%) the MRSA isolates were resistant to penicillin, 85(88.0%) to tetracycline, 61 (62.9%) to ciprofloxacin, 58 (60.0%) to erythromycin and 52 (53.6%) to gentamycin. The MRSA strains showed higher resistance rate than MSSA strains to all tested antibiotics. Multidrug resistance was found in 68.0% of the MRSA strains. Conclusion: There was high prevalence of MRSA with high rates of resistance to commonly used anti-staphylococcal antimicrobials, and a significant proportion of these MRSA isolates were multi-drug resistant. Vancomycin is the best choice for empiric treatment of suspected MRSA infections. Routine screening of clinical S. aureus isolates for methicillin resistance, regular surveillance studies as well as institution of infection control measures and antibiotic stewardship programme are recommended.
Keywords: Abuja, antibiotic susceptibility, methicillin-resistant Staphylococcus aureus, National Hospital Abuja, prevalence
|How to cite this article:|
Abdullahi N, Iregbu KC. Methicillin-Resistant Staphylococcus aureus in a Central Nigeria Tertiary Hospital. Ann Trop Pathol 2018;9:6-10
|How to cite this URL:|
Abdullahi N, Iregbu KC. Methicillin-Resistant Staphylococcus aureus in a Central Nigeria Tertiary Hospital. Ann Trop Pathol [serial online] 2018 [cited 2019 Mar 19];9:6-10. Available from: http://www.atpjournal.org/text.asp?2018/9/1/6/234154
| Introduction|| |
Methicillin-resistant Staphylococcus aureus (MRSA) is a significant cause of both healthcare-and community-associated infections globally with enormous clinical and economic impact.,, MRSA is due to the acquisition of mecA that is carried on a large mobile genetic element, the staphylococcal cassette chromosome, and which encodes a low affinity penicillin-binding protein 2a (PBP2a) to β-lactam antibiotics (except the fifth-generation cephalosporins).mecC when present may also mediate methicillin resistance. The mecA complex also contains insertion sites for plasmids and transposons that facilitate acquisition of resistance to other antibiotics (multidrug resistance [MDR]) such as erythromycin, clindamycin, gentamicin, cotrimoxazole, and ciprofloxacin., Consequently, options left for therapy are very few, expensive, and of limited availability, thereby making MRSA infections associated with poor outcome, prolonged hospital stay, increased cost of treatment, and increased morbidity and mortality.,, All these present a daunting challenge to virtually all healthcare institutions and policymakers in respect of the management of MRSA infections as well as its control. Tackling these challenges and ensuring quality of care in any healthcare environment requires good knowledge of the burden of MRSA infections and their antibiotic susceptibility pattern. This study was, therefore, carried out to fill this gap in knowledge in Abuja where there was no previous reliable study on MRSA and its antibiotic susceptibility and resistance pattern.
| Materials and Methods|| |
The study was conducted at National Hospital Abuja (NHA), Nigeria, between April 2014 and August 2015. All S. aureus isolates from routine clinical samples submitted to the medical microbiology laboratory of NHA within this period were included in this study. Identification of all isolates both morphologically and biochemically was done using standard laboratory methods. Briefly, all Gram-positive cocci in clusters that were positive to catalase, and coagulase tests were tentatively identified as S. aureus. They were confirmed by a positive result with mannitol fermentation and DNase tests.
Susceptibility testing was carried out on Mueller Hinton Agar (MHA) (Oxoid, Basingstoke, UK) plates using the modified Kirby–Bauer disc diffusion technique. The following antibiotic discs from oxoid were used: cefoxitin (30 μg), penicillin G (10 units), augmentin (20/10 μg), erythromycin (15 μg), tetracycline (30 g), gentamicin (10 μg), clindamycin (2 μg), vancomycin (30 μg), ciprofloxacin (5 μg), cefazolin (30 μg), cefuroxime (30 μg), ceftriaxone (30 μg), and imipenem (10 μg). Following this technique, a sterile cotton swab stick was used to inoculate the test organism onto the entire surface of MHA plate with the suspension of the test isolates equivalent to a 0.5 McFarland standard and then incubated at 35°C in ambient air for 18–24 h. The diameter of the zone of inhibition of each isolate to the tested antibiotics was measured in millimeters with a ruler and compared to the Clinical Laboratory and Standards Institute guideline (M100-S21) for interpretation., The isolates were considered methicillin resistant if the diameters of the zones of inhibition for cefoxitin were ≤21 mm and susceptible if ≥22 mm. S. aureus ATCC25923 (methicillin-susceptible S. aureus MSSA strain) and S. aureus ATCC 43300 (MRSA strain) were used as quality control strains. Collected data on patients' biodata, clinical sample type, point-of-care access/service units as well as the susceptibility and resistance profile of all the recovered S. aureus isolates were analyzed using the IBM-SPSS-version 18 (SPSS Inc., Chicago Inc I11, USA).
| Results|| |
Three hundred and sixty clinical strains of S. aureus were isolated from the various clinical specimens of patients submitted during the study. One hundred and eighty-one (50.3%) isolates were from males, while 179 (49.7%) were from females. One hundred and forty-one (39.2%) were from the age group of 0–14 years, 22 (6.1%) from the age group of 15–24 years and 197 (54.7%) from the age group of ≥25 years. Two hundred and thirteen (59.2%) of the S. aureus isolates were from inpatients, while 147 (40.8%) were from outpatients. One hundred and thirty-one (36.4%) of the isolates were from surgery units, 119 (33.1%) from pediatrics units, 53 (14.7%) from general outpatient department, 44 (12.2%) from internal medicine units, and 13 (14.7%) from other units [Table 1].
|Table 1: Overall demographics and baseline characteristics of sample population|
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All the 360 isolates were sensitive to vancomycin, 351 (97.5%) were susceptible to imipenem, 299 (83.1%) to cefazolin, 298 (82.8%) to clindamycin, and 281 (78.1%) to amoxicillin-clavulanic acid. Three hundred and thirty-one (91.9%) of the isolates were resistant to penicillin, 202 (56.1%) to tetracycline, and 163 (45.3%) to ceftriaxone [Table 2]. Ninety-seven (26.9%) of the 360 isolates were cefoxitin resistant (MRSA), while 263 (73.1%) were cefoxitin susceptible (MSSA) [Table 1] and [Table 2].
|Table 2: Antibiotic sensitivity pattern of Staphylococcus aureus isolates|
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Thirty-six (37.1%) of the MRSA isolates were from samples collected at the surgery units, 24 (24.7%) at the pediatrics units, and 15 (15.5%) at the internal medicine units. Sixty-one (62.9%) of the MRSA isolates were from inpatients, while 36 (37.1%) were from outpatients. Twenty-five (25.8%) of the MRSA isolates were from wound swabs, 24 (24.7%) from urine, and 22 (22.7%) from blood culture [Table 1]. All the 97 MRSA isolates were sensitive to vancomycin, 88 (90.7%) to imipenem, and 71 (73.2%) to clindamycin. All were resistant to penicillin, 92 (95.0%) to ceftriaxone, and 85 (88.0%) to tetracycline [Table 2]. Sixty-six (68.0%) of the MRSA isolates were MDR, while 34 (32.0%) were non-MDR [Table 3].
|Table 3: Multidrug-resistant isolates among methicillin-resistant Staphylococcus aureus and methicillin-susceptible Staphylococcus aureus|
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| Discussions|| |
The overall MRSA prevalence of 26.9% of S. aureus isolates in this study may be considered high although it falls within the range determined in a previous report of Gorwitz et al. which put the prevalence in Nigeria at the range of 21%–30%. Similar proportions of 28.6% and 28% have been reported from studies done in Kano and Bauchi, respectively., Some centers, however, had reported even higher rates of 34.7%, 43%, and 79% from Ilorin, Jos, and Benin, respectively.,, The use of methicillin disc for MRSA detection in these studies might have been responsible for the higher prevalence recorded in them. This is because hyperproducing penicillinase strains of S. aureus phenotypically give false-positive result for MRSA even in the absence of mecA and might have been falsely characterized as MRSA using methicillin for detection of MRSA. However, when compared to studies that used polymerase chain reaction PCR for mecA detection in southwestern Nigeria and Ekiti in particular which recorded prevalence of 22.2% and 19.2%, respectively,, the prevalence in this study is higher, particularly as this is the first available information on this in the hospital. As in other kinds of resistance, this may be connected with inappropriate use of antibiotics in the hospital, lack of antibiotics policy and guidelines and poor infection control practices.
The finding that almost two-thirds of the MRSA isolates were from inpatients corroborates previous studies that had demonstrated the predominance of MRSA in hospital environments.,,, This may be due to higher antibiotic consumption among hospitalized patients as well as the undoubtable role that the hospital environment plays in aiding the spread of MRSA. The existence of MRSA in the community suggests spread from the hospital through patients, healthcare workers, and probably visitors and tends to blur the distinctive profile of hospital strains from community strains. This has negative implication in the management of infections.
Wound swabs yielded the highest proportion of MRSA, and this had been established in previous studies.,,,, This was followed by urine and blood cultures in descending order. There is a breach in the skin epithelium in all wounds and is therefore more prone to infection than the intact skin. The expanding use of invasive procedures in tertiary hospital environment, including prosthetic devices, intravascular, and urinary catheterization, might have accounted for high yields from both blood culture and urine.
Although most of the MSSA isolates showed high susceptibility to amoxicillin/clavulanic acid in this study, the susceptibility to penicillin was low. Penicillin is cheap, commonly available over-the-counter and has been misused over the years. Motayo et al. and Fayomi et al. recorded similarly high rates in previous studies., Excellent and very poor susceptibility of these isolates to amoxicillin/clavulanic acid and penicillin, respectively, implied that beta-lactamase production was the main means of resistance among the isolates. This in effect identifies amoxicillin/clavulanic acid as a possible good choice for therapy of MSSA infections.
The characteristic MDR feature of MRSA was well observed in this study with respect to penicillin, tetracycline, ceftriaxone, ciprofloxacin, erythromycin, gentamicin, and cefuroxime. Previous studies elsewhere have made similar observation., The presence of insertion sites for plasmids and transposons in mecA complex of MRSA which often carry antibiotics resistance genes account for the resistance to several classes of antibiotics.
The high resistance of MRSA to ciprofloxacin, tetracycline, erythromycin, and gentamicin in this study has been confirmed by studies elsewhere ,, although studies in Kano, Ekiti, and Abeokuta have reported otherwise to ciprofloxacin and gentamycin. These drugs are commonly prescribed, available as over-the-counter antibiotics, and may have developed resistance due to selective pressure from inappropriate use.
Although MRSA displayed excellent susceptibility to imipenem, vancomycin, and clindamycin in this study, the nonutilization of MIC method to determine vancomycin susceptibility may have missed out some vancomycin intermediate S. aureus isolates among the 360 found susceptible using disc susceptibility testing method. Likewise, the nonperformance of D-test may have exaggerated the percentage susceptibility of the isolates to clindamycin, as some macrolide-induced clindamycin resistant strains might have been missed out. Elsewhere in Nigeria ,, and Michigan  similarly high susceptibility (88-100%) was reported for imipenem. The finding that all the MRSA isolates were susceptible to vancomycin have been reported by previous studies in Nigeria,,,, however, there are few reports of the emergence of vancomycin-resistant S. aureus in some centres in Nigeria., In addition, while previous study in Ekiti has documented similarly high MRSA susceptibility (74.5%) to clindamycin, reports from other studies still within the country recorded 92-94% sensitivity to the drug., Notwithstanding the aforementioned observations with respect to vancomycin and clindamycin, the display of excellent susceptibility of these isolates to imipenem, vancomycin, and clindamycin (if inducible resistance is not found with D-test) is good for therapeutic purposes, even as further studies are suggested to clear expressed doubts with respect to the susceptibilities recorded against the latter two drugs. These three drugs are not commonly in use in the hospital and so do not contribute significantly to selective pressure. They are also not readily available across the counter. The finding of clindamycin susceptibility in this study can be exploited in the treatment of skin and soft tissue infections, pneumonia, septic arthritis, and osteomyelitis in children caused by CA-MRSA as recommended in the Infectious Disease Society of American guidelines. This may be particularly useful in climes such as ours where vancomycin is not readily available.
Sixty-six (68.0%) of the MRSA isolates in this study were MDR-MRSA. This high prevalence of MDR-MRSA compares favorably with that recorded in Ido-Ekiti  but lower than that recorded in Benin and Zaria., This phenotypic characteristics seriously impairs therapeutic options, enhances spread, and increases morbidity and mortality.
From the findings of this work, vancomycin which is the only antibiotic with 100% susceptibility, even with multidrug resistant strains of MRSA, remains the best therapeutic option in our setting. Imipenem and clindamycin (in the absence of inducible resistance on D-test) are the alternatives for therapy of MRSA infections considering the high susceptibility of MRSA to these agents.
| Conclusion|| |
The study has shown high prevalence of MRSA with high rates of resistance to commonly available and used antimicrobials. There is therefore needed for both routine screening of all clinical S. aureus isolates for methicillin resistance and trend monitoring through regular surveillance studies. All the S. aureus isolates (MRSA and MSSA) remain sensitive to vancomycin, while the MRSA isolates were also highly susceptible to imipenem and clindamycin, respectively. Vancomycin should be used as the first empirical choice of treatment for serious MRSA infections in this environment, and to preserve its value, its use should be limited to those cases where they are clearly needed and as determined by laboratory susceptibility testing and/or recommended by treatment guidelines. Where vancomycin is not available, imipenem or clindamycin should be empirically used as alternatives for MRSA infections in that order. Institution of infection control measures and antibiotic stewardship will help in curtailing the emergence and spread of this resistant strain.
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Conflicts of interest
There are no conflicts of interest.
| References|| |
Kuehnert MJ, Hill HA, Kupronis BA, Tokars JI, Solomon SL, Jernigan DB, et al.
hospitalizations, United States. Emerg Infect Dis 2005;11:868-72.
Frazee BW, Lynn J, Charlebois ED, Lambert L, Lowery D, Perdreau-Remington F, et al.
High prevalence of methicillin-resistant Staphylococcus aureus
in emergency department skin and soft tissue infections. Ann Emerg Med 2005;45:311-20.
Stevens DL. Optimizing Outcomes in Methicillin-Resistant Staphylococcus aureus
Infections: Focus on Nosocomial Pneumonia and SSTI, Highlights from a Satellite Symposium at the 11th
Annual International Congress on Infectious Disease (ICID), Cancun, Mexico; 2004. p. 1-8.
Chambers HF. The changing epidemiology of Staphylococcus aureus
? Emerg Infect Dis 2001;7:178-82.
Que Y, Morreillon P. Staphylococcus aureus
(Including Toxic Shock Syndrome). In Mandell GL, Bennett JE, Dolin R, editors. Principles and Practice of Infectious Diseases. 7th
ed. Philadelphia, PA: Churchill Livingstone, An Imprint of Elsevier; 2010. p. 2543-78.
Miller LG. Managing an Elusive Pathogen: How Can MRSA be Contained? Clinical Updates from Medscape Infectious Diseases; 2010. Available from: http://www.medscape.org/Review Article
. [Last accessed on 2013 Feb 10].
Song JH, Hsueh PR, Chung DR, Ko KS, Kang CI, Peck KR, et al.
Spread of methicillin-resistant Staphylococcus aureus
between the community and the hospitals in Asian countries: an ANSORP study. J Antimicrob Chemother 2011;66:1061-9.
European Centre for Disease Prevention and Control. Antimicrobial Resistance Surveillance in Europe 2009. Annual Report of the European Antimicrobial Resistance Surveillance Network (EARS-Net). Stockholm, Sweden: ECDC; 2010.
Mejía C, Zurita J, Guzmán-Blanco M. Epidemiology and surveillance of methicillin-resistant Staphylococcus aureus
in Latin America. Braz J Infect Dis 2010;14 Suppl 2:S79-86.
Azeez OA, Utsalo SJ, Epoke J. Distribution and antibiotic susceptibility pattern of methicillin resistant Staphylococcus aureus
isolates in a University Teaching Hospital in Nigeria. Sahel Med J 2008;11:142-7.
Cheesbrough M. District Laboratory Practice in Tropical Countries. 2nd
ed. Cambridge, UK: Cambridge University Press; 2000. p. 64-7.
Clinical and Laboratory Standards Institute. Performance Standards for Antimicrobial Susceptibility Testing; Nineteenth Informational Supplement. Wayne PA: Clinical and Laboratory Standards Institute; 2009.
Clinical and Laboratory Standards Institute. Performance Standards for Antimicrobial Susceptibility Testing; Sixteenth Informational Supplement. Wayne PA: Clinical and Laboratory Standards Institute; 2006.
Gorwitz J, Jernigan DB, Powers JH, Jernigan JA, Participants in the CDC Convened Experts' Meeting on Management of MRSA in the Community. Strategies for Clinical Management of MRSA in the Community: Summary of Experts Meeting Convenes by the Centre for Disease Control and Prevention; March, 2006. USA. Available from: http://www.cdc.gov/ncidod/dhqp/ar_mrsa_ca.html
. [Last accessed on 2015 Jan 28].
Nwankwo BO, Abdulhadi S, Magagi A, Ihesiulor G. Methicillin-resistant Staphylococcus aureus
and their antibiotic susceptibility pattern in Kano, Nigeria. AfrJ Clin Exp Microbiol 2010;11:1595-689.
Ghamba PE, MangoroZM, Waza DE. Reoccurrence and distribution of methicillin resistant Staphylococcus aureus
(MRSA) in clinical specimens in Bauchi, North Eastern. Niger J Med Med Sci 2012;3:506-11.
Taiwo SS, Onile BA, Akanbi AA. Methicillin-resistant Staphylococcus aureus
(MRSA) isolates in Nigeria. Afr J Clin Exp Microbiol 2004;5:189-97.
Ikeh EI. Methicillin-resistant Staphylococcus aureus
(MRSA) at Jos teaching hospital. Afr J Cli Exp Microbiol 2003;4:52-5.
Onemu OS, Ophori EA. Prevalence of multi-drug resistant Staphylococcus aureus
in clinical specimens obtained from patients attending the university of Benin teaching Hospital, Benin City, Nigeria. J Nat Sci Res 2013;3:154-9.
Terry OA, Ogbolu DO, Akorede E, Onemu OM, Okanlawon BM. Distribution of mecA gene amongst Staphylococcus aureus
isolates from south western Nigeria. Afr J Biomed Res 2011;14:9-16.
Olowe OA, Kukoyi OO, Taiwo SS, Ojurongbe O, Opaleye OO, Bolaji OS, et al.
Phenotypic and molecular characteristics of methicillin-resistant Staphylococcus aureus
isolates from Ekiti state, Nigeria. Infect Drug Resist 2013;6:87-92.
Obianuju O, Babatunde O, Anthony O, Adesola O. The role of methicillin-resistant Staphylococcus aureus
in clinical infections in Obafemi Awolowo university teaching hospitals complex, Ile-Ife, South Western Nigeria. J Microbiol Exp 2015;2:41.
Jacobus CH, Lindsell CJ, Leach SD, Fermann GJ, Kressel AB, Rue LE, et al.
Prevalence and demographics of methicillin resistant Staphylococcus aureus
in culturable skin and soft tissue infections in an urban emergency department. BMC Emerg Med 2007;7:19.
Fayomi OD, Oyediran EI, Adeyemo AT, Oyekale OT. Resistance pattern of methicillin-resistance Staphylococcus aureus
among in-patients at a tertiary health facility in Ido-Ekiti, Nigeria. Internet J Lab Med 2011;4:1-5. [Doi: 10.5580/30b].
Shittu AO, Lin J. Antimicrobial susceptibility patterns and characterization of clinical isolates of Staphylococcus aureus
in Kwa Zulu-natal province, South Africa. BMC Infect Dis 2006;6:125.
Okon KO, Basset A, Uba P, Oyawoye OM, Yusuf IZ, Shittuand AO. Epidemiology and characteristic pattern of methicillin-resistant Staphylococcus aureus
recovered from tertiary hospitals in Northeastern, Nigeria. Int J Trop Med 2011;6:106-12.
Mohanty S, Kapil A, Dhawan B, Das BK. Bacteriological and antimicrobial susceptibility profile of soft tissue infections from Northern India. Indian J Med Sci 2004;58:10-5.
] [Full text]
Majumder D, Bordoloi JS, Phukan AC, Mahanta J. Antimicrobial susceptibility pattern among methicillin resistant Staphylococcus
isolates in Assam. Indian J Med Microbiol 2001;19:138-40.
] [Full text]
Motayo BO, Akinduti PA, Okerentugba PO, Innocent-Adiele HC, Onoh CC, Nwanze JC, et al
. Methicillin resistance and beta-lactamase production in Staphylococcus aureus
isolated from different clinical samples in Abeokuta, Nigeria. Acad Arena 2012;4:25-9.
Nworie A, Azi SO, Ibiam GA, Egwu IH, Udoh I, Okereke EC, et al
. Nasal carriage of methicillin resistant Staphylococcus aureus
amongst meat sellers in Abakaliki Metropolis, Ebonyi State, Nigeria. Microbiol Res Int 2013;1:48-53.
Ayeni FA, Olatunji DF, Ogunniran M. Prevalence of methicillin resistant Staphylococcus aureus
and resistance pattern of its clinical strains to beta-lactam antibiotics. Afr J Biomed Res 2014;17:129-33.
Iyamba JM, Wambale JM, Lukukula CM, za Balega Takaisi-Kikuni N. High prevalence of methicillin resistant staphylococci strains isolated from surgical site infections in Kinshasa. Pan Afr Med J 2014;18:322.
Fan W, del Busto R, Love M, Markowitz N, Cendrowski C, Cardenas J, et al.
Imipenem-cilastatin in the treatment of methicillin-sensitive and methicillin-resistant Staphylococcus aureus
infections. Antimicrob Agents Chemother 1986;29:26-9.
Kesah C, Ben Redjeb S, Odugbemi TO, Boye CS, Dosso M, Ndinya Achola JO, et al.
Prevalence of methicillin-resistant Staphylococcus aureus
in eight African hospitals and malta. Clin Microbiol Infect 2003;9:153-6.
Taiwo SS, Bamigboye TB, Odaro O, Adefioye OA, Fadiora SO. Vancomycin intermediate and high level resistant Staphylococcus aureus
clinical isolates in Osogbo, Nigeria. Microbiol Res 2011;3:22-5.
Onolitola OS, Olayinka BO, Salawu MJ, Yakubu SE. Nasal carriage of methicillin resistant Staphylococcus aureus
with reduced vancomycin susceptibility (MRSA-RVS) by healthy adults in Zaria, Nigeria. J Trop Microbiol Biotechnol 2007;3:19-22.
Nwankwo EO, Nasiru MS. Antibiotic sensitivity pattern of Staphylococcus aureus
from clinical isolates in a tertiary health institution in Kano, North Western Nigeria. Pan Afr Med J 2011;8:4.
Liu C, Bayer A, Cosgrove SE, Daum RS, Fridkin SK, Gorwitz RJ, et al.
Clinical practice guidelines by the infectious diseases society of America for the treatment of methicillin-resistant Staphylococcus aureus
infections in adults and children. Clin Infect Dis 2011;52:e18-55.
Adebola O, Avosuahi RO, Josiah AO. Prevalence and susceptibility pattern of methicillin resistant Staphylococcus aureus
isolates among healthy women in Zaria, Nigeria. Afr J Biotechnol 2005;4:1321-4.
[Table 1], [Table 2], [Table 3]