Mupirocin-resistant Staphylococcus aureus in Africa: a systematic review and meta-analysis

Shittu, Adebayo O.; Kaba, Mamadou; Abdulgader, Shima M.; Ajao, Yewande O.; Abiola, Mujibat O.; Olatimehin, Ayodele O.

doi:10.1186/s13756-018-0382-5

Table 2 Characteristics of the 43 eligible studies on screening for mupirocin resistance in Staphylococcus aureus from various sources in Africa

From: Mupirocin-resistant Staphylococcus aureus in Africa: a systematic review and meta-analysis

Region	Country	Study Period	Setting	Sample		Method for testing resistance to mupirocin	Guideline (year of publication)	Published reports for detection of mupR S. aureus	Number of S. aureus isolates screened with mupirocin	Mupirocin resistant isolates				Reference
Region	Country	Study Period		Source	Type	Method for testing resistance to mupirocin	Guideline (year of publication)	Published reports for detection of mupR S. aureus	Number of S. aureus isolates screened with mupirocin	Number (%)	Number MRSA (%)	Number LmupR/HmupR	Number mupA gene + LMupR/HmupR (Method)	Reference
North Africa	Algeria	2005–2007	C & H	Human	Pus, venous catheter, tracheal aspirate, punction fluid, blood, urine	Disk diffusion VITEK-2	CLSI (NA)	–	19	0 (0)	0 (0)	–	–	[47]
	Egypt	2005–2006	C & H	Human	NA	Disk diffusion	NCCLS (2003)	–	64	0 (0)	0 (0)	–	–	[28]
	Egypt	2008–2009	C & H	Human	Skin and soft tissue, post-operative wound swab	Disk diffusion	CLSI (2007)	–	386	1 (0.3)	NA	NA	–	[29]
	Egypt	2007–2008	C	Human	Pus, sputum, catheter, blood, urine, wound abscess	Broth dilution	CLSI (2005)	–	21	0 (0)	0 (0)	–	–	[58]
	Egypt	2010	H	Human	Sputum, blood, catheter, traumatic wound, urine	E-test	–	Kresken et al., (2004)	86	30 (34.9)	30 (34.9)	25/5	2/3 (PCR)	[30]
	Egypt	2012	H	Human	Wound discharge, blood, body fluid aspirate, urine, faeces, sputum, nasal, throat, ear and genital swab	Disk diffusion Agar dilution	CLSI (2007)	–	150	0 (0)	0 (0)	–	–	[40]
	Egypt	2012–2013	H	Human	Nasal swab	Disk diffusion	CLSI (2011)	–	39	3 (7.7)	3 (3.7)	NA	–	[31]
	Egypt	2013–2015	H	Human	Pus & Wound swab	Agar dilution	CLSI (2011)	–	73	13 (17.8)	13 (17.8)	5/8	0/6 (PCR)	[52]
	Libya	NA	H	Human	Skin swab	Disk diffusion	NA	–	40	0 (0)	NA	–	–	[61]
	Libya	2008–2009	H	Human & Environment	NA	Disk diffusion	BSAC (2008)	–	86	13 (15.1)	13 (8.1)	NA	–	[56]
	Libya	2009	H	Human	Nasal swab	Disk diffusion Agar dilution	BSAC (2008)	–	109	5 (4.6)	5 (4.6)	4/1	–	[57]
	Morocco	2008-	H	Human	Nasal swab	Disk diffusion	CA-SFM (2007)	–	81	0 (0)	0 (0)	–	–	[62]
	Tunisia	2008–2009	C	Human	Nasal swab	Disk diffusion	CLSI (2008)	–	55	0 (0)	0 (0)	–	–	[41]
	Tunisia	2003–2005	C	Human	Pus, blood, articular puncture, venous catheter	Phoenix Automated Microbiology System	CA-SFM (2006)	–	64	NA	NA	–	–	[59]
	Tunisia	2013	H	Human	Wound abscess	Disk diffusion	CA-SFM (2013)	–	8	NA	NA	–	–	[60]
	Tunisia	2010	C	Animal (Sheep)	Nasal swab	Disk diffusion	CLSI (2010)	–	73	0 (0)	0 (0)	–	–	[42]
	Tunisia	2010	C	Animal (Donkeys)	Nasal swab	Disk diffusion	CLSI (2010)	–	50	0 (0)	0 (0)	–	–	[43]
West Africa	Ghana	2011–2012	H	Human	Nasal swab	Disk diffusion	EUCAST (2012)	–	105	1 (0.9)	0 (0)	0/1	–	[54]
	Ghana	2011–2012	C	Human	Nasal swab	Disk diffusion	EUCAST (2012)	–	124	0 (0)	0 (0)	–	–	[67]
	Ghana	2010–2013	C & H	Human	NA	Broth microdilution	EUCAST (NA)	–	30	4 (13.3)	4 (13.3)	4/0	0/0 (DNA microarray)	[55]
	Ghana	2012–2013	C	Human	Nasal & Wound swab	VITEK-2	EUCAST (NA)	–	91	0 (0)	0 (0)	–	–	[68]
	Nigeria*	NA	NA	Human	NA	Disk diffusion	NA	–	1	0 (0)	0 (0)	–	–	[80]
	Nigeria*	2002–2004	H	Human	Wound, blood, ear, eye, urine	Disk diffusion	–	Udo et al., (1999)	200	1 (0.5)	0 (0)	0/1	0/1 (PCR)	[53]
	Nigeria	2006	C	Human	Nasal swab	Disk diffusion	CLSI (2005)	–	101	12 (11.9)	NA	NA	–	[44]
	Nigeria	2007	H	Human	NA	Disk diffusion	CLSI (NA)	–	96	0 (0)	0 (0)	–	–	[48]
	Nigeria*	NA	H	Human	Wound swab, blood, urine, endotracheal aspirate	Disk diffusion E-test	NCCLS (2003)	–	1	1	0 (0)	0/1	0/1 (PCR)	[45]
	Nigeria	2009	H	Human	Wound, sputum, semen, nasal swab	Broth microdilution	DIN 58940 (2004)	–	68	0 (0)	0 (0)	–	–	[63]
	Nigeria	2010	H	Human	NA	VITEK-2	–	–	51	0 (0)	0 (0)	–	–	[64]
	Nigeria	2009–2011	H	Human	Aspirate, blood, ear, eye, vaginal discharge, sputum, wounds, urine, nasal swab	Disk diffusion	CLSI (NA)	–	62	0 (0)	0 (0)	–	–	[49]
	Nigeria	2010–2011	H	Human	NA	VITEK-2	EUCAST (NA)	–	290	0 (0)	0 (0)	–	–	[65]
	Nigeria	2008–2010	C	Animal (Bats)	Faecal swab	Disk diffusion	–	Udo et al., (1999)	107	0 (0)	0 (0)	–	–	[66]
	Nigeria	2006–2007	C & H	Animal (Bovine) & (Ovine)	Nasal & skin swab	Disk diffusion	–	Udo et al., (1999)	173	0 (0)	0 (0)	–	–	[35]
	Nigeria	2012	C	Human Animal	Nasal swab Milk	Disk diffusion	CLSI (2006)	–	10 Humans 77 Animals	33 (37.9)	NA	0/33	–	[36]
Central Africa	Gabon	2009	C & H	Human	Nasal, axillae, inguinal swab	VITEK-2	–	–	5	0 (0)	0 (0)	–	–	[69]
Central Africa	São Tomé & Príncipe	2010–2012	H	Human	Nasal swab	Disk diffusion	BSAC (NA)	–	55	0 (0)	0 (0)	–	–	[70]
East Africa	Ethiopia	NA	H & R	Cockroach	Cockroach Body surface/Gut	Disk diffusion	–	Jorgenson et al., (1999)	17	17 (100)	NA	NA	–	[37]
	Kenya	2011	H	Human	Nasal and axillary skin swab	VITEK-2	CLSI (2012)	–	86	0 (0)	0 (0)	–	–	[71]
	Kenya	2011–2013	H	Human	Pus, blood, urine	VITEK-2	CLSI (2010)	–	731	0 (0)	0 (0)	–	–	[72]
	Kenya	NA	C	Animal (Camel)	Raw camel milk	Disk diffusion Broth microdilution	CLSI (2008)	–	47	0 (0)	0 (0)	–	–	[38]
South Africa	South Africa	1996	H	Human	Wound, urine, skin and blood	Disk diffusion	NCCLS (2000)	–	236	5 (2.1)	NA	NA	–	[46]
	South Africa**	2001–2003	H	Human	Wound, sputum, blood	Disk diffusion	–	Udo et al., (1999)	227	16 (7.0)	15 (6.6)	14/2	0/2 (PCR)	[50]
	South Africa	2005–2006	H	Human	Blood, pus & skin wound, cerebrospinal fluid	Disk diffusion E-test	–	Udo et al., (2006)	248	123 (49.6)	123 (49.6)	117/6	–	[32]
	South Africa**	NA	H	Human	Wound swab, blood, urine, endotracheal aspirate	Disk diffusion E-test	NCCLS (2003)	–	16	16 (100)	14 (87.5)	14/2	0/2 (PCR)	[45]
	South Africa	2013	H	Human	Tissue, blood, cerebrospinal fluid, wound swab	Disk diffusion VITEK-2	CLSI (2012)	–	997	277 (27.8)	NA	43/234	0/5 (Real time PCR)	[33]
	South Africa	2010–2012	H	Human	Blood	Microscan (MIC Panel Type 33)	CLSI (2015)	–	2709	236 (8.7)	202 (7.5)	NA	–	[51]
	South Africa	2009–2010	H	Human & Environment	Nasal & hand swab, dialysate fluid, surface swab, air samples	VITEK-2	–	–	13	4 (30.8)	4 (30.8)	0/4	–	[34]

KEY: mupR S. aureus: mupirocin resistant Staphylococcus aureus; LmupR low-level mupirocin resistance, HmupR high-level mupirocin resistance, mupA mupirocin resistance gene, MIC Minimum inhibitory concentration, BSAC British Society for Antimicrobial Chemotherapy, CA-SFM Comité de l’Antibiogramme de la Société Française de Microbiologie, CLSI Clinical and Laboratory Standards Institute, DIN 58940 Deutsches Institut für Normung DIN 58940, EUCAST European Committee on Antimicrobial Susceptibility Testing, NCCLS National Committee for Clinical Laboratory Standards, PCR Polymerase Chain Reaction; − Not determined, NA Not available, H Hospital, C Community, R Restaurant
*Separate reports that analyzed the same isolates but answered different questions (considered as one single study) in Nigeria; **: Separate reports that analyzed the same isolates but answered different questions (considered as one single study) in South Africa.
Reference [45] is recorded in Nigeria and South Africa, but the isolates were derived from studies in Nigeria [53] and South Africa [50], respectively
Other published reports applied for the detection of mupR S. aureus in Africa
1. Jorgenson JH, Turnidge JD, Washington JA. Dilution and disc diffusion method. In: Murray PR, Baron EJ, Pfaller MA, Tenover FC, Yolken RH, editors. Manual of Clinical Microbiology, 7th edition. American Society for Microbiology, Washington DC, 1999. p. 1526–1543. Adapted from NCCLS: National Committee for Clinical Laboratory Standards 1997. Approved Standard M2-A6; National Committee for Clinical Laboratory Standards 1999. Approved Standard M100-S9.
2. Kresken M, Hafner D, Schmitz FJ, Wichelhaus TA. Prevalence of mupirocin resistance in clinical isolates of Staphylococcus aureus and Staphylococcus epidermidis. Results of the antimicrobial resistance surveillance study of the Paul-Ehrlich Society for Chemotherapy, 2001. Int J Antimicrob Agents, 2004, 23:577–81. The widely accepted breakpoints: ≤4 mg/l (susceptible), 8–256 mg/l (low-level resistance) and ≥ 512 mg/l (high-level resistance) was utilized in this study.
3. Udo EE, Farook VS, Mokadas EM, Jacob LE, Sanyal SC. Molecular fingerprinting of mupirocin-resistant methicillin-resistant Staphylococcus aureus from a burn unit. Int J Infect Dis, 1999,3:82–7. Growth within a 14-mm zone of inhibition with the 5 μg mupirocin disk detected low-level resistance, while growth to the edge of the 200 μg mupirocin disk indicated high-level resistance.
4. Udo EE, Al-Sweih N, Mokaddas E, Johny M, Dhar R, Gomaa HH, Al-Obaid I, Rotimi VO. Antibacterial resistance and their genetic location in MRSA isolated in Kuwait hospitals, 1994–2004. BMC Infect Dis, 2006;6:168. The widely accepted breakpoints:≤4 mg/l (susceptible), 8–256 mg/l (low-level resistance) and ≥ 512 mg/l (high-level resistance) was utilized in this study.

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