ESBL-producing Enterobacteriaceae in Africa - a non-systematic literature review of research published 2008-2012.

INTRODUCTION: Enterobacteriaceae producing extended-spectrum beta-lactamases (ESBL) has been found all over the world, and risk factors for acquiring these bacteria involve hospital care and antibiotic treatment. Surveillance studies are present in Europe, North America, and Asia, but there is no summarizing research published on the situation in Africa. AIM: This review aims to describe the prevalence of ESBL-producing Enterobacteriaceae in hospital and community settings in Africa and the ESBL genes involved.
METHOD: A non-systematic literature search was performed in PubMed. All articles published between 2008 and 2012 were screened and read in full text. Relevant articles were assessed for quality of evidence and included in the review. Articles were divided into regional areas in Africa and tabulated.
RESULTS: ESBL-producing Enterobacteriaceae in hospitalized patients and in communities varies largely between countries and specimens but is common in Africa. ESBLs (class A and D) and plasmid-encoded AmpC (pAmpC) were regularly found, but carbapenemases were also present.
CONCLUSION: ESBL-producing Enterobacteriaceae in hospital and community settings in Africa is common. Surveillance of antimicrobial resistance needs to be implemented in Africa to tailor interventions targeted at stopping the dissemination of ESBL-producing Enterobacteriaceae.

Research has shown that there are several risk factors for acquiring an extended-spectrum beta-lactamase (ESBL)-producing bacterial infection. High use of antibiotics is one factor that has been shown to increase the risk of developing and acquiring ESBL for patients at hospitals and in the community (1–4). Nosocomial risk factors, such as the presence of intravascular catheters, undergoing surgery, staying at an intensive care unit, and international travel, have been shown to increase the risk of being colonized with ESBL-producing bacteria (1, 3, 5).

Introduction

ESBL has been found all over the world, and reviewing research has been done in Europe (6, 7), North America (8), and Asia (9) in recent years to understand the extent of ESBLs and other multiresistant bacteria; also, there are surveillance studies running in the same regions to guide the clinical treatment of infectious diseases. In Europe (during 1999–2008), there has been an increase in invasive infections caused by Klebsiella pneumoniae and Escherichia coli resistant to third-generation cephalosporins, and this is believed to be due to the dissemination of ESBLs in both hospitals and communities. An increase in carbapenemase production among isolates has also been seen and raises issues regarding future antimicrobial treatment (10). Urinary tract isolates collected in the SMART study between 2009 and 2010 concluded that in Europe, ESBL prevalence among E. coli and K. pneumoniae was 17.6 and 38.9%, respectively. In North America, the prevalence was 8.5 and 8.8%, respectively (11). In Asia, the prevalence of ESBL among E. coli and K. pneumoniae varied between 5 and 0%, respectively, in New Zealand and between 67 and 61%, respectively, in China (12). The class A ESBL gene CTX-M-15 was the most common gene in the European and American settings (found in >90% of E. coli isolates and in 35–65.5% of K. pneumoniae), but SHV- and TEM-type genes were also prevalent, between 1.7 and 42.9%, especially in K. pneumoniae (11). From the SENTRY Asia Pacific surveillance program, CTX-M genes were found in 38.2–55.5% of K. pneumoniae and E. coli isolates, and the prevalence of SHV- and TEM-type genes was higher (between 34.3 and 85.3%) (13).

In Africa, the prevalence of ESBL in Enterobacteriaceae has been researched at local levels in various countries, but there is no summarizing research on how prevalent ESBL is on the continent, what type of genes are involved, and where research is missing. This review aims to describe the prevalence of ESBL-producing Enterobacteriaceae in hospital and community settings in Africa and the ESBL genes involved.

Method

A literature search was conducted in PubMed in June 2013 with the keywords ‘Africa’, ‘Enterobacteriaceae’, and ‘ESBL’ or ‘extended-spectrum beta-lactamases’. The search was limited to articles published in English, studying humans, and published from 2008/01/01 to 2012/12/31. From the 91 references found, seven articles could not be accessed in online databases or acquired in paper copy, and they were excluded; the remaining 84 articles were read in full text. 19 articles were excluded because they were not relevant for the aim of this study. The excluded articles did not research ESBL, studied countries outside of Africa, or looked at other colonized hosts than humans. 65 articles were finally included in the review.

The references were assessed in quality according to a value scale, modified from Hedin et al. (14), where the strength of evidence for different ESBL genes and prevalence in the selected references were graded low, middle, and high based on the method of analyses used in the studies. As many of the studies reported had used the same method, study size and what proportion of the sample was analyzed in detail were also taken into account to assess the strength of the scientific evidence (Table 1).

Table 1

Value scale used for assessing strength of evidence

Grade		Criteria
High	Method	Polymerase chain reaction (PCR)
		Plasmid transfer assays (PTA)
		Pulsed field gel electrophoresis (PFGE)
	Sample size	>15
		Data set completely analyzed
Middle		Combination of criteria from high and low grade (e.g., sample <15 but using PCR analyses)
Low	Method	Synergy tests
	Sample size	<15
		Data set partly analyzed

Results

This section is divided into regional areas of Africa, according to the UN regional composition (15). For detailed descriptions of sample sizes, organisms, settings and prevalence, sources of samples, and ESBL genes involved, see Tables 2–6.

Table 2

Northern Africa

Country (study period)	Sample size	Organism	Setting and prevalence of ESBL (%)	Source of ESBL isolate (%)	Genes (%)	Evidence	Reference
Algeria (1982–2005)	12	S. Enterica serotype Senftenberg	Hospital	Not specified	Exemplary 1 isolate:	Low	(20)
			(n/r)		TEM-1 (100)
					CTX-M-3 (100)
Algeria (2003–2007)	141	E. cloacae	Hospital	Urine (52)	CTX-M-15 (44)	High	(17)
			(17.7)	Blood (24)	CTX-M-3 (36)
				Pus (24)	SHV-12 (16)
					VEB (4)
Algeria (2003–2007)	505	Enterobacteriaceae	Hospital	Urine (63.6)	CTX-M group I (84.3)	Middle	(16)
			(16.4)	Blood (18.2)	TEM (15.7)
				Pus (18.2)	SHV (15.7)
					CMY-2 (9.6)
					DHA-1 (3.6)
Algeria (2005)	3	K. pneumoniae	Hospital	Pus (33.3)	CTX-M-15 (66.6)	Middle	(22)
			(n/r)	Cerebrospinal fluid (33.3)	CTX-M-3 (33.4)
				Urine (33.3)	TEM-1 (100)
					SHV-98 (33.3)
					SHV-99 (33.3)
					SHV-100 (33.4)
Algeria (2008–2009)	200	S. Enterica serotype Infantis	Hospital	Stool (88.2)	Exemplary 16 isolates:	High	(19)
			(99)	Blood (5.9)	CTX-M-15 (100)
				Gastric fluid (5.9)	TEM-1 (100)
Algeria (2009)	207	Klebsiella	Hospital	Urine (53.7)	Exemplary 41 isolates:	High	(12)
		Enterobacter	(31.4)	Pus (19.5)	CTX-M group I (88)
		Serratia		Distal sampling (14.6)	TEM (41.4)
				Valve (2.4)	SHV (31.1)
				Pleural fluid (2.4)	DHA-1 (9.7)
				Ear (2.4)
				Nasal fossae (2.4)
				Tumoral fluid (2.4)
Algeria (not specified)	196	K. pneumoniae	Hospital	Urine (38.9)	Exemplary 18 isolates:	High	(18)
			(19.9)	Blood (22.2)	TEM (100)
				Bronchial (13.6)	CTX-M-3 (66.7)
				Pus (13.6)	CTX-M-15 (33.3)
				Ascites fluid (5.9)
Egypt (2007)	70	E. coli	Hospital and community	Stool (not specified)	Exemplary 8 isolates:	Middle	(24)
			(42.9)	Urine (not specified)	CTX-M-1 (75)
					CTX-M-9 (87.5)
Egypt (2007–2008)	520	Enterobacteriaceae	Hospital	Urine (78.7)	Exemplary 74 isolates:	Middle	(23)
			(19)	Wound (10.6)	CTX-M-15 (100)
			Community	Ascites fluid (4.3)	SHV-12 (1.4)
			(11)	Sputum (6.4)
Egypt (not specified)	5	K. pneumoniae	Hospital	Wound (80)	CTX-M-14 (40)	Middle	(25)
		E. coli	(n/r)	Catheter (20)	CTX-M-15 (20)
		E. cloacae			TEM (20)
					SHV (20)
Guinea-Bissau (2010)	408	K. pneumoniae	Hospital	Stool (100)	CTX-M group I (94.8)	High	(26)
		E. coli	(32.6)		CTX-M group 9 (4)
					CTX-M group 8/25 (0.8)
					CTX-M group 2 (0.8)
					SHV (2.3)
Libya (2011)	25	Enterobacteriaceae	Hospital	Rectal (100)	Exemplary 1 isolate	Middle	(27)
			(16)		OXA-48 (100)
Morocco (2004–2007)	535	E. coli	Community	Urine (100)	CTX-M-15 (100)	High	(33)
			(1.3)		TEM-1 (28.6)
					SHV-5 (14.3)
Morocco (2004–2009)	803	K. pneumoniae	Community	Urine (100)	CTX-M-15 (91.7)	High	(31)
		E. coli	(1.5)		TEM-1b (33.3)
					SHV-1 (16.7)
					SHV-5 (8.3)
					OXA-1 (91.7)
Morocco (2006–2007)	39	Enterobacteriaceae	Hospital	Urine (66.7)	Exemplary 14 isolates:	Middle	(28)
			(n/r)	Pus (10.3)	TEM-1 (85.7)
				Bronchial (2.6)	CTX-M-28 (35.7)
				Blood (7.7)	CTX-M-15 (25)
					SHV-12 (35.7)
					SHV-1 (25)
					DHA-1 (58.3)
Morocco (2010)	453	K. pneumoniae	Community	Urine (100)	CTX-M-15 (94.1)	High	(32)
			(7.5)		CTX-M-1 (2.9)
					TEM-1 (52.9)
					TEM-1b (29.4)
					SHV-1 (35.3)
					SHV-11 (11.8)
					SHV-12 (8.8)
					SHV-26 (5.9)
					SHV-28 (8.8)
					SHV-32 (2.9)
					SHV-36 (2.9)
					SHV-76 (5.9)
					SHV-110 (2.9)
					OXA-1 (64.7)
					ACT-2 (2.9)
					DHA-1 (2.9)
Morocco (not specified)	3	K. pneumoniae	Hospital	Urine (33.3)	NDM-1 (100)	Middle	(29)
			(n/r)	Blood (33.3)	CTX-M-15 (100)
				Abscess (33.4)	TEM-1 (100)
					SHV-1 (100)
					SHV-5 (100)
					OXA-1 (100)
					OXA-9 (100)
Morocco (not specified)	3	K. pneumoniae	Hospital	Not specified	NDM-1 (100)	Low	(30)
			(n/r)		CTX-M-15 (100)
					OXA-1 (100)
Tunisia (1999–2005)	1280	K. pneumoniae	Hospital	Urine (41.2)	51 exemplary isolates (hospital):	High	(42)
			(11.7)	Lung (11.8)	CTX-M-15 (37.3)
			Community	Catheter (7.8)	CTX-M-27 (3.9)
			(0.7)	Cerebrospinal fluid (3.9)	SHV-12 (62.8)
				Blood (25.5)	SHV-2a (5.9)
				Pus (3.9)	TEM-1 (19.6)
				Nasal (3.9)
				Rectal (2)
Tunisia (2003–2007)	11	K. pneumoniae	Hospital	Urine (27.3)	CTX-M-15 (100)	High	(34)
		E. coli	(n/r)	Sputum (18.2)	SHV-1 (54.6)
				Blood (36.4)	SHV-11 (9.1)
				Pus (9.1)	SHV-27 (9.1)
				Catheter (9.1)	SHV-103 (9.1)
					TEM-1a (54.6)
					TEM-1b (36.4)
					OXA-1 (72.7)
Tunisia (2004)	1	K. pneumoniae	Hospital	Not specified	CTX-M-28 (100)	Low	(36)
			(n/r)
Tunisia (2004)	1	P. mirabilis	Hospital	Not specified	VEB-1 (100)	Low	(48)
			(n/r)
Tunisia (2004)	1	K. pneumoniae	Hospital	Not specified	TEM-164 (100)	Low	(35)
			(n/r)
Tunisia (2005–2006)	856	Enterobacteriaceae	Hospital	Urine (58)	100 exemplary isolates:	High	(40)
			(19.9)	Blood (42)	CTX-M-15 (93)
					TEM-1 (82)
					SHV-12 (9)
					SHV-2a (7)
					OXA-1 (92)
Tunisia (2005–2007)	281	Enterobacteriaceae	Hospital	Urine (63.9)	36 exemplary isolates:	Middle	(41)
			(n/r)	Blood (36.1)	CTX-M-15 (69.4)
					SHV-28 (13.9)
					SHV-12 (5.6)
					SHV-2a (2.8)
					TEM-1 (77.8)
					LAP-2 (5.6)
Tunisia (2005–2009)	20	P. stuartii	Hospital	Blood (53.5)	VEB-1a (100)	Middle	(47)
			(n/r)	Trachea (33.3)
				Pus (6.7)
				Chest drainage (6.7)
Tunisia (2006)	47	E. coli	Hospital	Urine (34.4)	CTX-M-15 (96.9)	High	(51)
			(68.1)	Stool (31.3)	TEM-1b (81.3)
				Intra-abdominal peritonitis (9.4)	TEM-34 (9.4)
				Trachea (6.3)	SHV-12 (6.3)
				Blood (6.3)
				Pus (6.3)
				Wound (3.1)
				Lung (3.1)
Tunisia (2007)	14	E. coli	Hospital	Urine (64.3)	CTX-M-15 (85.7)	Middle	(38)
			(n/r)	Blood (7.1)	CTX-M-14a (7.1)
				Wound (28.6)	CTX-M-14b (7.1)
					OXA-1 (85.7)
					TEM-1 (35.7)
Tunisia (2008)	1	M. morganii	Hospital	Pus (100)	CTX-M-15 (100)	Low	(49)
			(n/r)		TEM-24 (100)
					DHA-1 (100)
Tunisia (2009)	44	E. cloacae	Hospital	Urine (59.9)	CTX-M-15 (88.6)	High	(34)
			(n/r)	Pus (20.5)	TEM-1 (77.3)
				Blood (9.1)	SHV-12 (13.6)
				Broncho-pulmonary (4.6)	SHV-27 (2.3)
				Gastric (4.6)
				Catheter (2.3)
Tunisia (2009)	1	P. stuartii	Hospital	Rectal (100)	TEM-116 (100)	Low	(45)
			(n/r)
Tunisia (2009–2010)	9	E. cloacae	Hospital	Urine (57.1)	SHV-12 (100)	Low	(44)
			(n/r)	Placenta (28.6)
				Blood (14.3)
Tunisia (2009–2010)	150	E. coli	Community	Stool (100)	CTX-M-1 (90.9)	High	(37)
			(7.3)		TEM-1b (9.1)
					TEM-52c (9.1)
Tunisia (2010)	2	K. pneumoniae	Hospital	Urine (100)	CTX-M-15 (100)	Low	(46)
			(77.8)		TEM-1 (100)
					SHV-1 (100) OXA-48 (100)
Tunisia (2010)	10	E. coli	Hospital	Urine (100)	CTX-M-15 (100)	High	(39)
			(n/r)		TEM-52 (100)
Tunisia (2011)	11	P. stuartii	Hospital	Nose (45.5)	OXA-48 (100)	Middle	(50)
			(n/r)	Rectal (27.3)	CMY-4 (100)
				Axilla (27.2)	PER-1 (100)

n/r: not relevant.

Table 6

Southern Africa

Country (study period)	Sample size	Organism	Setting and prevalence of ESBL (%)	Source of ESBL isolate (%)	Genes (%)	Evidence	Reference
South Africa (2001)	59	Salmonella	Hospital	Stool (100)	TEM-1 (50.9)	High	(80)
			(n/r)		TEM-63 (20.3)
					TEM-116 (13.3)
					TEM-131 (3.3)
					SHV-12 (50)
					CTX-M-15 (6.7)
					CTX-M-34 (3.3)
					CTX-M-3 (3.3)
					CTX-M-37 (16.7)
					OXA-1 (3.3)
					CMY-2 (10)
South Africa (2002–2003)	181	Enterobacteriaceae	Hospital	Nasopharyngeal (100)	Not analyzed	Middle	(75)
			(8.8)
South Africa (2003–2009)	6,833	Shigella	Community	Stool (80)	CTX-M-15 (90)	High	(79)
			(0.3)	Blood (20)	CTX-M-14 (5)
					TEM-1 (80)
					SHV-2 (5)
					CMY-2 (30)
South Africa (2004–2009)	1,019	Enterobacteriaceae	Hospital	Wound (100)	Not analyzed	Middle	(74)
			(10.8)
South Africa (2005–2006)	1,125	Enterobacteriaceae	Hospital	Urine (100)	Not analyzed	Middle	(77)
			(13.1)
			Community
			(4.7)
South Africa (2007)	46	Enterobacteriaceae	Hospital	Not specified	TEM (95.7)	Middle	(76)
			(n/r)		SHV (58.7)
					CTX-M (54.4)
					Exemplary 10 isolates of CTX-M:
					CTX-M-15 (100).
South Africa (2008–2009)	22	E. coli	Hospital	Urine (77.3)	CTX-M-15 (59.1)	High	(78)
			(n/r)	Pus (22.7)	CTX-M-14 (31.8)
					CTX-M-3 (4.6)
					SHV-2 (4.6)
					TEM-1 (54.6)
					TEM-2 (4.6)
					OXA-1 (40.9)

n/r: not relevant.

Northern Africa

In Algerian hospitals, ESBLs existed in 16.4–31.4% of the samples. Class A ESBLs were most common, but plasmid-encoded AmpC (pAmpC) was also present (16–22).

In Egypt, ESBLs were found in 11–42.9% of samples in both hospitals and communities; the genes involved were class A ESBLs (23–25).

In Guinea-Bissau and Libya, class A and D ESBLs and a carbapenemase were found in 32.6 and 16%, respectively, in rectal or stool samples (26, 27).

In Morocco, class A and D ESBLs, pAmpC, and carbapenemases were found in hospital settings (28–30). In the community setting, class A and D ESBLs were found in between 1.3 and 7.5% of acquired urine samples (31–33).

In Tunisia, class A and D ESBLs, pAmpC, and carbapenemases were present, and the prevalence ranged from 11.7 to 77.8% in hospitals and was 0.7 and 7.3% in two communities (34–51).

Eastern Africa

In Ethiopia and Kenya, 62.8 and 37.4%, respectively, of hospital and community samples were ESBLs (52, 53). Class A ESBLs and pAmpC were present in the Kenyan sample (53. In samples taken from Kenya and Malawi, class A and D ESBLs were found (54).

In Rwanda, ESBLs were found in 38.3% of hospital urine samples and in 5.9% of community urine samples (55).

In Tanzania, class A ESBLs were found in various samples from hospital settings (56, 57).

Central Africa

In Cameroon, class A and D ESBLs were found in 55.3 and 82.8% of hospital stool samples and in 17.2% of community stool samples (58, 59).

In the Central African Republic, ESBLs were found in 11.3% of community urine samples (60).

Western Africa

In Ghana and Mali, class A ESBLs were found in 49.4 and 63.4–96%, respectively, in hospital and community samples (61–64).

In Niger, 40% of hospital samples carried class A ESBLs or pAmpC (65).

In Nigeria, class A and D ESBLs and pAmpC were found in hospital settings, and the prevalence ranged from 10.3 to 27.5% (66–71). In a mixed sample from a hospital and a community, the prevalence was 11.7% (72).

In Senegal, class A and D ESBLs were found in 10% of community stool samples (73).

Southern Africa

In South Africa, class A and D ESBLs and pAmpC were present, and the prevalence ranged from 8.8 to 13.1% in hospitals and was 0.3 and 4.7% in two communities (74–80).

Discussion

This review indicates that ESBL-producing Enterobacteriaceae are a large problem in African healthcare institutions and communities.

In patients treated in African hospitals, the prevalence of ESBL-producing Enterobacteriaceae has been shown to vary between countries and the type of specimen studied. There is a trend of higher prevalence of ESBL in stool samples than in other specimens. There is also a trend of increasing prevalence over time. This is noticeable in the Tunisian setting, where a large amount of studies are available. In two hospitals studied (study periods: 1999–2005 and 2010), ESBLs have increased from 11.7 to 77.8% among K. pneumoniae (42, 49). In other settings, the trend is not noticeable among the few studies available. In the studied countries in Africa, the prevalence is widely different: in Algeria, it was between 16.4 and 31.4% in mainly urine samples (16–18, 21) and even 99% among Salmonella enterica in stool samples (19); 19 and 42.9%, respectively, in urine and stool samples in Egypt (23, 24); 32.6% among stool samples in Guinea-Bissau (26); 11.7–77.8% in mainly urine, blood, and stool samples from Tunisia (40, 42, 46, 51); 62.8% in stool and blood samples from Ethiopia (52; 38.3% in urine samples from Rwanda (55); 55.3 and 82.8% in stool samples from Cameroon (58, 59); 10.3–27.5% in mainly urine and stool samples from Nigeria (66, 69–72); and 8.8–13.1% in urine, nasopharyngeal, and wound samples from South Africa (74, 75, 77).

The most common type of genes involved in the African hospital strains of ESBL is class A ESBLs. CTX-M-15 is the most prevalent gene in a high proportion of the samples, disregarding country. It is usually combined with other types of CTX-M, TEM, and SHV genes (17–19, 22, 25, 28, 29, 34, 38, 40–43, 46, 51, 53, 56–59, 65–67, 69, 70, 78). There is a high proportion of class D ESBLs existent, mainly OXA-1, and it has been found in between 3.3 and 93.3% of the studied isolates (34, 38, 40, 53, 54, 58, 59, 67, 69, 78, 80). pAmpC genes exist in some isolates, mainly DHA-1 and CMY-2 (16, 18, 21, 28, 29, 32, 49, 50, 53, 65, 69, 79), but because of the different classifications of ESBLs, these are not always included in the analyses performed in the studies. Disturbing results are the existence of carbapenemase genes. The NDM-1 gene was found in three samples taken from urine, blood, and an abscess from two patients in Morocco (29, 30), and the OXA-48 gene was found in a rectal swab sample from a patient originating from Libya (27). The presence of carbapenemase genes is a risk for future use of antimicrobial treatment in the region.

In the community setting, ESBL-producing Enterobacteriaceae have a lower prevalence than in the hospital: 6.7% of healthy students in Cameroon (58), 1.3% in a Moroccan community (33), 5.9% in Rwandan outpatients (55), 2.7% in a healthy community in Nigeria (72), 11.3% of outpatients in Central African Republic (60), 10% of healthy children in a remote village in Senegal (73), and 4.7% in a referral site in South Africa (77). The genes involved in the community were the same as in the hospital setting.

To solve the problem of ESBL-producing Enterobacteriaceae and other types of resistant bacteria, prevention is crucial and surveillance of antimicrobial resistance is needed to guide prevention interventions. Because of globalization, including international travel, it is important to have a global approach to antibiotic resistance. The majority of the studies in this review are performed in northern or southern Africa, leaving a large gap in the areas in between. Future research should focus on areas where research is scarce, describing the current situation in healthcare services and increasing the consistent surveillance to follow the changes in prevalence and incidence, making relevant interventions possible on both local and global levels.

Conclusion

ESBLs (class A and D) are common in Africa, with the gene CTX-M-15 being most prevalent, but other types, such as pAmpC and carbapenemases, also exist. Surveillance of antimicrobial resistance needs to be implemented in Africa to tailor interventions targeted at stopping the dissemination of ESBL-producing Enterobacteriaceae.

Table 3

Eastern Africa

Country (study period)	Sample size	Organism	Setting and prevalence of ESBL (%)	Source of ESBL isolate (%)	Genes (%)	Evidence	Reference
Ethiopia (2004–2006)	113	Salmonella	Hospital	Stool (68)	Not analyzed	Middle	(52)
			(62.8)	Blood (32)
Kenya (1992–2010)	912	E. coli	Hospital and community	ESBL:	140 exemplary isolates ESBL:	High	(53)
			(37.4)	Urine (53)	CTX-M-14 (29)
				Stool (26)	CTX-M-15 (24)
				Blood (21)	CTX-M-1 (6)
					CTX-M-3 (11)
				pAmpC:	CTX-M-9 (2)
				Urine (72)	CTX-M-8 (4)
				Stool (14)	TEM-52 (16)
				Blood (14)	SHV-5 (3)
					SHV-12 (5)
					94 exemplary isolates pAmpC:
					OXA-12 (66)
					CMY-1 (18)
					CMY-2 (82)
Kenya and Malawi (not specified)	18	S. typhimurium	Hospital	Blood (100)	OXA-1 (100)	High	(54)
			(n/r)		TEM-1 (100)
Rwanda (2009)	196	Enterobacteriaceae	Hospital	Urine (100)	Not analyzed	Middle	(55)
			(38.3)
			Community
			(5.9)
Tanzania (2009–2010)	17	Enterobacteriaceae	Hospital	Blood (100)	CTX-M-15 (100)	Medium	(56)
			(n/r)
Tanzania (not specified)	32	E. coli	Hospital	Wound (34.3)	CTX-M-15 (100)	High	(57)
			(n/r)	Urine (25)	TEM-1 (25)
				Pus (21.9)
				Blood (18.8)

n/r: not relevant.

Table 4

Central Africa

Country (study period)	Sample size	Organism	Setting and prevalence of ESBL (%)	Source of ESBL isolate (%)	Genes (%)	Evidence	Reference
Cameroon (2009)	121	Enterobacteriaceae	Hospital	Stool (100)	CTX-M-15 (96)	High	(59)
			(55.3)		SHV-12 (4)
					SHV-1 (25)
					TEM-1 (79)
					OXA-1 (65)
Cameroon (2009)	358	Enterobacteriaceae	Hospital	Stool (100)	CTX-M-15 (98)	High	(58)
			(82.8)		CTX-M-1 (2)
			Community		TEM-1 (67)
			(17.2)		SHV-1 (4)
					SHV-12 (3)
					OXA-1 (58)
Central African Republic (2004–2006)	443	Enterobacteriaceae	Community	Urine (100)	Not analyzed	Middle	(60)
			(11.3)

n/r: not relevant.

Table 5

Western Africa

Country (study period)	Sample size	Organism	Setting and prevalence of ESBL (%)	Source of ESBL isolate (%)	Genes (%)	Evidence	Reference
Ghana (2008–2009)	156	E. coli	Hospital and community	Urine (not specified)	CTX-M (not specified)	Middle	(61)
			(49.4)	Blood (not specified)	TEM (not specified)
				Sputum (not specified)	SHV (not specified)
				Wound (not specified)
				Aspirates (not specified)
Mali (2001–2008)	41	Salmonella	Community	Stool (100)	CTX-M-15 (19.2)	High	(62)
			(63.4)		TEM-1 (96.2)
					SHV-12 (80.8)
Mali (2002–2005)	25	Enterobacteriaceae	Community	Stool (100)	Exemplary 52 isolates:	High	(63)
			(96)		CTX-M-15 (80.8)
					SHV-12 (7.7)
					SHV-2 (1.9)
					TEM-1 (78.8)
Mali (2003)	68	Enterobacteriaceae	Community	Stool (100)	Not analyzed	Middle	(64)
			(83.3)
Niger (2007–2008)	55	Enterobacteriaceae	Hospital	Stool (100)	CTX-M-15 (90.1)	High	(65)
			(40)		SHV-2a (9.1)
					SHV-12 (9.1)
					SHV-44 (4.6)
					CMY-2 (4.6)
					CMY-30 (4.6)
Nigeria (1999)	1	E. aerogenes	Hospital	Blood (100)	AmpC (100)	Low	(68)
			(n/r)		TEM-1 (100)
					SHV-12 (100)
Nigeria (2005–2007)	134	Enterobacteriaceae	Hospital	Sputum (not specified)	TEM (81.3)	High	(69)
			(20.9)	Ear (not specified)	SHV (24.6)
				Wound (not specified)	OXA (11.2)
				Throat (not specified)	CTX-M-15 (17.9)
				Vaginal (not specified)	CTX-M-3 (0.8)
				Eye (not specified)
				Aspirates (not specified)	Exemplary 6 isolates:
				Urine (not specified)	DHA-1 (66.7)
				Blood (not specified)	ACT-1 (16.7)
				Catheter (not specified)	CMY-2 (16.6)
				Cerebrospinal fluid (not specified)
Nigeria (2006–2007)	116	E. coli	Hospital	Urine (66.7)	Exemplary 9 isolates:	High	(70)
			(10.3)	Stool (25)	CTX-M-15 (100)
				Blood (8.3)
Nigeria (2006–2007)	44	E. coli	Hospital	Urine (77.2)	CTX-M group I (100)	Middle	(67)
			(n/r)	Vaginal (13.6)	3 exemplary isolates CTX-M-15 (100)
				Wound (9.0)	TEM (93.1)
					OXA-1 (93.1)
Nigeria (2006–2007)	145	Enterobacteriaceae	Community and hospital	Urine (82.4)	Not analyzed	Middle	(72)
			(11.7)	Vaginal (11.8)
				Wound (5.9)
Nigeria (2007–2008)	153	Salmonella	Hospital	Stool (100)	Not analyzed	Middle	(71)
		Shigella	(27.5)
Nigeria (2008–2009)	109	E. coli	Hospital	Urine (35.7)	CTX-M-15 (100)	High	(66)
			(12.8)	Stool (21.4)
				Wound (21.4)
				Semen (7.1)
				Blood (7.1)
				Catheter (7.1)
Senegal (not specified)	20	E. coli	Community	Stool (100)	CTX-M-15 (100)	High	(73)
			(10)		TEM-1 (100)
					OXA-1 (100)

n/r: not relevant.