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. 2013 Aug;57(8):3628–3639. doi: 10.1128/AAC.00359-13

Evaluation of Antimicrobial Susceptibility of Enterobacteriaceae Causing Urinary Tract Infections in Africa

Giannoula S Tansarli a, Stavros Athanasiou a,c, Matthew E Falagas a,b,d,✉
PMCID: PMC3719698  PMID: 23689709

Abstract

Our objective was to evaluate the antimicrobial susceptibility of Enterobacteriaceae causing urinary tract infections (UTIs) in adults in Africa. The PubMed database was systematically searched to identify relevant studies published after 2000. Google, World Health Organization, and African Field Epidemiology networks were also searched. Twenty-eight studies, accounting for 381,899 urine isolates from 14 African countries, met the inclusion criteria. Escherichia coli, Klebsiella spp., and Proteus spp. were the most commonly encountered uropathogens. Cefotaxime, imipenem, fosfomycin, and ciprofloxacin were the antibiotics with the highest activity against E. coli isolates from outpatients, with susceptibility being 92 to 99, 100, 100, and 68 to 91%, respectively. The susceptibility among Klebsiella spp. isolates from outpatients varied from 80 to 100% for amikacin and from 53 to 100% for ciprofloxacin, while susceptibility was 74 to 78, 97, and 77% for ciprofloxacin, amikacin, and fosfomycin, respectively, among Klebsiella species isolates from inpatients or patients with hospital-acquired UTIs. With regard to Proteus spp., the highest activity was observed among fluoroquinolones; 71 to 100% of the P. mirabilis isolates were susceptible to ciprofloxacin in four studies, and 74 to 100% of the P. vulgaris isolates were susceptible to ofloxacin in two studies. The currently available evidence suggests that the antimicrobial susceptibility patterns of Enterobacteriaceae uropathogens in African countries were similar to those in countries of southeast Europe. Further original studies are warranted from African countries for which there is limited published data.

INTRODUCTION

UTIs are among the most commonly encountered infections, both in the community and in hospitals. Escherichia coli, Klebsiella spp., and Proteus spp. are the uropathogens with the highest prevalence among patients with UTIs. However, the antibiotic susceptibility patterns of Enterobacteriaceae have been constantly changing due to the continuous development of new resistance mechanisms, like the production of extended-spectrum beta-lactamases or carbapenemases by bacteria and the spread of genes on mobile elements. Antimicrobial susceptibility studies on uropathogens have been performed in many countries around the world, upgrading the medical management of patients with UTIs (1–10).

Africa is a continent where financial resources for the health care system are low in many countries, especially in those in sub-Saharan Africa. Accordingly, antibiotics may be lacking and the quality of health care may be suboptimal. The investigation of the antimicrobial resistance of Enterobacteriaceae uropathogens in the developing countries of Africa would optimize the treatment options used for patients with UTIs. Additionally, knowledge of antimicrobial resistance in these countries would be of great interest, since large numbers of Africans migrate to countries of the developed world, affecting the local antimicrobial susceptibility patterns. In this context, we aimed to systematically review and evaluate the available evidence in order to delineate the antimicrobial susceptibility of Enterobacteriaceae causing UTIs in Africa.

MATERIALS AND METHODS

Abbreviations.

BLs, beta-lactams; FQs, fluoroquinolones; AGs, aminoglycosides; SXT, trimethoprim-sulfamethoxazole; NTF, nitrofurantoin; FOS, fosfomycin; abx, antibiotics; NR, not reported; NA, nonapplicable; MC, multicenter; ESBL, extended-spectrum beta-lactamase; MDR, multidrug resistant; HIV, human immunodeficiency virus; IP, inpatients; OP, outpatients; UTI, urinary tract infection; AFENET, African Field Epidemiology Network; WHO, World Health Organization; Amp, ampicillin; Amc, amoxicillin-clavulanic acid; Amx, amoxicillin; Pen, penicillin; Mec, mecillinam; Tic, ticarcillin; Ticc, ticarcillin-clavulanic acid; Pip, piperacillin; Tzp, piperacillin-tazobactam; Cephs, cephalosporins; Ctx, cefotaxime; Ctxc, cefotaxime-clavulanic acid; Czd, ceftazidime; Ctrx, ceftriaxone; Cfpm, cefepime; Cth, cephalothin; Cfx, cefuroxime; Cxt, cefoxotin; Cxm, cefixime; Clx, cephalexin; Czl, cefazolin; Cb, carbenicillin; Cfm, cefamandole; Ctt, cefotetan; Cam, chloramphenicol; Tet, tetracycline; Tpm, trimethoprim; Imi, imipenem; Mer, meropenem; Azt, aztreonam; Gen, gentamicin; Amk, amikacin; Tob, tobramycin; Net, netilmicin; Sm, streptomycin; Cipro, ciprofloxacin; Nal, nalidixic acid; Pfx, pefloxacin; Nor, norfloxacin; Ofx, ofloxacin; Ntx, nitroxoline; Lvf, levofloxacin; Erm, erythromycin; Azi, azithromycin; Coli, colistin; Su, sulfonamide.

Literature search.

The PubMed database was systematically searched in November 2012. The following search phrase was applied to all articles published after 2000: “(enterobacteriaceae OR klebsiella OR proteus OR escherichia OR e. coli OR enterobacter) AND (urinary tract infection OR uti) AND (Africa)”. In addition, the following keywords were applied to the Google search engine during the same period for articles also published after 2000, “enterobacteriaceae,” “escherichia coli,” “klebsiella,” “proteus,” “enterobacter,” “providencia,” “serratia,” “citrobacter,” “morganella,” “urinary tract infection,” “uti,” “susceptible,” “susceptibility,” “resistance,” and “Africa.” The WHO network, AFENET, and the bibliographies of all eligible articles were also searched in order to identify additional potentially eligible studies. Lastly, articles published in languages other than English, German, French, Spanish, Italian, or Greek were not evaluated, because they were considered to be of suboptimal quality.

Study selection.

Articles providing the antimicrobial susceptibility pattern of more than 15 isolates of Enterobacteriaceae collected from adult patients with clinically or microbiologically documented or suspected UTI were considered eligible for inclusion in the review. Both clinical and microbiological (in vitro) studies including isolates recovered from patients meeting the aforementioned criteria were eligible. Studies reporting on neonates, children, or adolescents were excluded. In addition, studies evaluating patients with asymptomatic bacteriuria were also excluded.

Data extraction.

The extracted data consisted of the first author, year of publication, period of the study, country, study design, number of patients, and main patient characteristics. In addition, the prevalence of all causative pathogens of UTIs as well as the susceptibility of Enterobacteriaceae to all antibiotics tested in each study was also recorded. The included studies were stratified primarily according to pathogen and the origin of the study population (outpatients, inpatients, both, or undetermined origin).

Definitions and outcomes.

Antimicrobial susceptibility of Enterobacteriaceae was defined according to the susceptibility breakpoints used by the investigators of each of the included studies. Isolates exhibiting intermediate susceptibility to an antibiotic were considered resistant. For the purposes of the study, patients with community-acquired UTIs were classified as outpatients, and those with hospital-acquired UTIs were classified as inpatients.

The outcome of the review was the antimicrobial susceptibility of Enterobacteriaceae causing UTIs to major classes of antibiotics.

RESULTS

The electronic search of the PubMed database generated 191 articles. Twenty-eight articles from PubMed, Google, WHO, and AFENET, as well as results of manually searching the bibliographies of relevant studies, accounting for 381,899 urine isolates (both Gram-negative and Gram-positive bacteria), met the criteria for inclusion in the review. The detailed process of the study selection is depicted in Fig. 1.

Fig 1.

Fig 1

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Flow diagram of the detailed study selection process.

Data originated from 14 countries, South Africa, Nigeria, Senegal, Morocco, Tunisia, Libya, Algeria, Central African Republic, Kenya, Zimbabwe, Rwanda, Sudan, Madagascar, and Mauritius. The antimicrobial susceptibility data reported on >1,000 isolates of Enterobacteriaceae for the following countries: South Africa (358,930) (11, 12), Tunisia (8,890) (13–15), Nigeria (3,070) (16–23), and Senegal (2,102) (24–26). In 13 studies, the antimicrobial susceptibility was defined according to the Clinical and Laboratory Standards Institute guidelines (11, 12, 16, 17, 20, 22, 23, 27–32), while in 10 other studies the guidelines of the Comité de l' Antibiogramme de la Société Française de Microbiologie were used (13–15, 24–26, 33–36). The susceptibility breakpoints that were used were not provided in 5 studies (18, 19, 21, 37, 38). Seventeen of the included studies had a prospective nature (12, 16–19, 21–23, 26, 27, 29–32, 35, 37, 38), while 11 had a retrospective nature (11, 13–15, 20, 25, 28, 33, 34, 36). The characteristics and outcomes of the included studies are presented in Tables 1, 2, and 3.

Table 1.

Characteristics and outcomes of the included studies reporting on outpatients

Bacterial isolate(s) and data source Study design; period, country Total no. of isolates; characteristics Prevalence (%) of the studied pathogen Susceptibility (%) of Enterobacteriaceae isolates to:
BLs FQs AGs SXT NTF FOS Other abx
Escherichia coli
    Bourjilat et al. (27) Prospective cross-sectional; 2004–2007, Morocco 535; E. coli isolates from patients in a community setting; 1.3% ESBL producing NA Amx, 0; Amc, 0; Tic 0; Cth, 0; Cxt, 100; Czd, 0; Cfpm, 0; Imi, 100 (ESBL) Cipro, 29; Nal, 29 (ESBL) Gen, 14; Tob, 0; Amk, 86 (ESBL) 0 (ESBL) NR 100 (ESBL) NR
    Dromigny et al. (25) Retrospective cohort; 1999–2000, Senegal 1,266 38.6 Amp, 30; Amc, 75; Tic, 31; Cth, 75; Cxt, 98; Ctx, 99 Nal, 92; Pfx,a 91; Nor, 93 Gen, 98; Tob, 99; Amk, 100 40 NR NR Tet, 22; Cam,a 68
    Dromigny et al. (24) Prospective cohort; 2001–2003, Senegal 398; consecutive E. coli isolates from patients with acute infection; 6.3% ESBL producing NA Amp, 26; Amc, 42; Tic, 29; Cth, 52; Cxt, 89; Ctx, 93; Imi, 100 FQs,b 81; Nal, 77 Gen, 93; Tob, 91; Amk, 99 37 NR NR Tet, 24; Cam, 72
    Hima-Lerible et al. (34) Retrospective cohort; 2000–2002, Central African Republic 313 55.6 Amx, 18; Amp, 26; Tic, 20; Pip, 27; Mec, 45; Cth, 44; Ctrx, 100; Czd, 100 Cipro, 90; Nal, 90; Ntx, 21 Gen, 94; Tob, 94; Amk, 100; Net, 96 15 NR 98 NR
    Isaack et al. (38) Prospective cohort; 2005, Mauritius 260 46.5 Amp, 20; Amc, 45; Mec, 83; Clx, 88; Ctx, 92; Cxm, 89 Cipro, 69; Nal, 63 Gen, 90 41 76 100 NR
    Kariuki et al. (30) Prospective cohort; 2004–2005, Kenya 17; fluoroquinolone-resistant E. coli isolates from patients with community-acquired UTIs; 71% ESBL producing NA Amp, 0; Amc, 0; Czd, 0; Ctx, 0; Ctrx, 0; Cxt, 0; Imi, 100; Mer, 100 (ESBL); Amp, 0; Amc, 0; Ctx, 100; Ctrx, 100; Czd, 100; Cfpm100; Cxt, 0; Imi, 100; Mer, 100 (non-ESBL) Nal, 0; Cipro, 0; Lvf, 0 (ESBL); Nal, 0; Cipro, 0; Lvf, 0 (non-ESBL) Gen, 0 (ESBL) and 100 20 (non-ESBL) 0 (ESBL) and 0 (non- ESBL) NR Tet, 0 (ESBL)
    Mbanga et al. (31) Prospective cohort; NR, Zimbabwe 62; isolates from patients with suspected UTI 40.3 Amp, 16 Cipro, 68; Nal, 52; Ntx, 100 Gen, 64 32 84 NR Tet, 52
    Nadmi et al. (35) Prospective cohort; 2008, Morocco 100; isolates from private laboratories 80 Amx, 39; Amc, 86; Cxt, 94; Cfpm, 100; Czd, 97; Ctx, 96; Imi, 100; Azt, 99 Nal, 73; Cipro, 80 Kan, 80; Tob, 86; Gen, 91; Amk, 100 66 NR NR Tet, 57
    Nwadioha et al. (20) Retrospective cohort; 2007–2008, Nigeria 910 51 Amp, 49; Ctrx, 98 Cipro, 99; Nal, 53 Gen, 72 46 70 NR Tet, 38
    Randrianirina et al. (36) Retrospective cohort; 2004–2006, Madagascar 903; isolates from patients with community-acquired infections 67.2 Amx, 23; Amc, 45; Tic, 23; Cth, 45; Cfm, 47; Cxt, 93; Ctrx, 95; Czd, 95 Cipro, 84; Nal, 75; Ntx, 1 Gen, 91; Tob, 82; Amk, 98; Net, 96 27 NR 100 NR
    Sire et al. (26) Prospective cohort; 2004–2006, Senegal 1,010; E. coli isolates from patients with community-acquired UTIs; 3.8% ESBL producing NA Amx, 27; Amc, 32; Tic, 32; Cth, 44; Ctx, 96; Czd, 96 (all E. coli) Nal, 76; Cipro, 84; Nor, 84 Gen, 94 32 90 99 NR
Klebsiella spp.
    Dromigny et al. (25) Retrospective cohort; 1999–2000, Senegal 1,266 9.1 K. pneumoniae Amp, 0; Amc, 75; Tic, 0; Cth, 79; Cxt, 90; Ctx, 91 Nal, 94; Pfx,a 97; Nor, 97 Gen, 91; Tob, 90; Amk, 100 53 NR NR Tet, 43; Cam,a 69
    Isaack et al. (38) Prospective cohort; 2005, Mauritius 260 13.8 Klebsiella spp. Amp, 0; Amc, 36; Mec, 81; Clx, 81; Ctx, 81; Cxm, 74 Cipro, 53; Nal, 53 Gen, 67 56 37 100 NR
    Kehinde et al. (19) Prospective cohort; 2007–2009, Nigeria 118; isolates from pregnant women 38.1 K. oxytoca Cxm, 78 Ofx, 93; Nal, 84 Gen, 84 NR 78 NR NR
    Nadmi et al. (35) Prospective cohort; 2008, Morocco 100; isolates from private laboratories 13 Klebsiella spp. Amx, 0; Amc, 69; Cxt, 77; Cfpm, 100; Czd, 100; Ctx, 100; Imi, 100; Azt, 100 Cipro, 100; Nal, 92 Kan, 85; Tob, 100; Gen, 100; Amk, 100 54 NR NR Tet, 69
    Nwadioha et al. (20) Retrospective cohort; 2007–2008, Nigeria 910 19.6 Klebsiella spp. Amp, 49; Amc, 53; Czd, 89 Cipro, 95; Nal, 51 Gen, 70 0 51 NR Tet, 49
    Soge et al. (23) Prospective cohort; 2002–2003, Nigeria 30; K. pneumoniae MDR isolates from patients with community-acquired infections NA Amp, 0; Pip, 10; Tzp, 53; Ctx, 43; Ctxc, 100; Czl, 33; Czd, 40; Ctrx, 43; Cfpm, 43; Ctt, 100; Imi, 100; Azt, 43 NR NR NR NR NR NR
Other Enterobacteriaceaec or on the total isolates of Enterobacteriaceae of a study
    Bercion et al. (33) Retrospective cohort; 2004–2006, Central African Republic 560; ESBL-producing isolates; 3.7, 8.9, and 19.3% Enterobacteriaceae in 2004, 2005, and 2006, respectively 64 Escherichia coli, 10 K. pneumoniae, 2 Salmonella spp., 1.8 Proteus spp., 0.5 Enterobacter spp., 0.7 Citrobacter spp., 0.2 Morganella morganii, 21 other bacteria Amx, 12; Amc, 46; Cth, 58; Ctx, 82 (all); Amx, 12; Amc, 42; Cth, 61; Ctx, 98 (ESBL) Nal, 65; Nor, 69; Cipro, 70; Ntx, 17 (all); Nal, 67; Nor, 72; Cipro, 74; Ntx, 15 (ESBL) Gen, 79 (all); Gen, 83 (ESBL) 14 (all); 16 (ESBL) NR 97 (all); 99 (ESBL) NR
    Dromigny et al. (25) Retrospective cohort; 1999–2000, Senegal 1,266 2.3 Enterobacter spp., 4.8 other Enterobacteriaceae Amo, 0; Amc, 0; Tic, 48; Cth, 0; Cxt, 0; Ctx, 76 (Enterobacter spp.); Amp, 25; Amc, 67; Tic, 44; Cth, 66; Cxt, 77; Ctx, 97 (other Enterobacteriaceae) Nal, 57; Pfx,a 58; Nor, 66 (Enterobacter spp.); Nal, 92; Pfx,a 92; Nor, 93 (other Enterobacteriaceae) Gen, 83; Tob, 79; Amk, 97 (Enterobacter spp.); Gen, 95; Tob, 92; Amk, 97 (other Enterobacteriaceae) 48 (Enterobacter spp.); 70 (other Enterobacteriaceae) NR NR Tet, 24 (Enterobacter spp.) and 34 (other Enterobacteriaceae); Cam,a 50 (Enterobacter spp.) and 46 (other Enterobacteriaceae)
    Hima-Lerible et al. (34) Retrospective cohort; 2000–2002, Central African Republic 313 28.8 other Enterobacteriaceaed Amx, 1; Amc, 29; Tic, 5; Pip, 29; Mec, 39; Cth, 48; Ctrx, 99; Czd, 99 (other Enterobacteriaceae) Cipro, 91; Nal, 88; Ntx, 16 Gen, 85; Tob, 89; Amk, 100; Net, 89 23 NR 90 NR
    Isaack et al. (38) Prospective cohort; 2005, Mauritius 260 21.2 Proteus spp. and other Enterobacteriaceae Amp, 16; Amc, 47; Mec, 86; Clx, 80; Ctx, 91; Cxm, 84 (Proteus spp. and other Enterobacteriaceae) Cipro, 71; Nal, 69 Gen, 91 55 63 97 NR
    Kehinde et al. (19) Prospective cohort; 2007–2009, Nigeria 118; isolates from pregnant women 9.3 P. mirabilis, 2.6 P. vulgaris Cxm, 63 (P. mirabilis); Cxm, 100 (P. vulgaris) Ofx, 88; Nal, 75 (P. mirabilis); Ofx, 100; Nal, 67 (P. vulgaris) Gen, 75 (P. mirabilis) and 67 (P. vulgaris) NR 63 (P. mirabilis) and 67 (P. vulgaris) NR NR
    Mbanga et al. (31) Prospective cohort; NR, Zimbabwe 62; isolates from patients with suspected UTI 30 Enterobacteriaceae other than E. colid Amp, 15 (Enterobacteriaceae other than E. coli) Cipro, 54; Nal, 23; Ntx, 100 Gen, 38 31 54 NR Tet, 61
    Nadmi et al. (35) Prospective cohort; 2008, Morocco 100; isolates from private laboratories 6 Enterobacter cloacae, 1 Providencia spp. Amx, 0; Amc, 67; Cxt, 67; Cfpm, 100; Ctx, 100; Czd, 100; Imi, 100; Azt, 100 (E. cloacae); Amx, 100; Amc, 100; Cxt, 100; Cfpm, 100; Ctx, 100; Czd, 100; Imi, 100; Azt, 100 (Providencia spp.) Nal, 83; Cipro, 83 (E. cloacae); Nal, 100; Cipro, 100 (Providencia spp.) Kan, 83; Tob, 83; Gen, 100; Amk, 100 (E. cloacae); Kan, 100; Tob, 100; Gen, 100; Amk, 100 (Providencia spp.) 50 (E. cloacae) and 100 (Providencia spp.) NR NR Tet, 67 (E. cloacae) and 100 (Providencia spp.)
    Nwadioha et al. (20) Retrospective cohort; 2007–2008, Nigeria 910 10 P. mirabilis, 7.1 P. vulgaris Amp, 48; Amc, 53; Ctrx, 96 (P. mirabilis); Amp, 49; Amc, 53; Ctrx, 98 (P. vulgaris) Cipro, 96; Nal, 53 (P. mirabilis); Cipro, 95; Nal, 51 (P. vulgaris) Gen, 72(P. mirabilis) and 71 (P. vulgaris) 48 (P. mirabilis) and 46 (P. vulgaris) 62 (P. mirabilis) and 53 (P. vulgaris) NR Tet, 47 (P. mirabilis) and 46 (P. vulgaris)
    Randrianirina et al. (36) Retrospective cohort; 2004–2006, Madagascar 903; isolates from patients with community-acquired infections 18.7 other Enterobacteriaceaed Amx, 12; Amc, 48; Tic, 24; Cth, 48; Cfm, 52; Cxt, 73; Ctrx, 90; Czd, 90 (other Enterobacteriaceae) Cipro, 88; Nal, 78; Ntx, 97 Gen, 89; Tob, 77; Amk, 96; Net, 67 46 NR 86 NR
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a

Susceptibility testing was performed for these antibiotics in only 1 of the 2 years of the study period.

b

Fluoroquinolones included ciprofloxacin, pefloxacin, and norfloxacin.

c

The term “other Enterobacteriaceae” refers to Enterobacteriaceae strains other than E. coli and Klebsiella spp. or strains other than those reported in each study.

d

In these studies, the group “other Enterobacteriaceae” includes Klebsiella spp. as well.

Table 2.

Characteristics and outcomes of the included studies reporting on inpatients

Isolate(s) and data source Study design; period, country Total no. of isolates Prevalence of the studied pathogen Susceptibility of Enterobacteriaceae (%) to:
BLs FQs AGs SXT NTF FOS Other abx
Escherichia coli
    Nwadioha et al. (20) Retrospective cohort; 2007–2008, Nigeria 910 51% Amp, 35; Amc, 45; Ctrx, 81 Cipro, 86; Nal, 44 Gen, 48 38 53 NR Tet, 38
Klebsiella spp.
    Ben Haj Khalifa et al. (13) Retrospective survey; 2009, Tunisia 3,564 6% Klebsiella spp. (198 isolates; 188 K. pneumoniae and 10 K. oxytoca (ESBL producing); 20% Klebsiella spp. (40 isolates) Amc, 60; Ctx, 66 (all); Amc, 0; Ctx, 0 (ESBL) Cipro, 74; Nal, 48; OFX, 73 (all); Cipro, 32; Nal, 20; Ofx, 32 (ESBL) Gen, 69; Tob, 70; Amk, 97 (all); Gen, 7; Tob, 10; Amk, 90 (ESBL) 57 (all); 27 (ESBL) 68 (all); 47 (ESBL) 77 (all); 82 (ESBL) NR
    Nwadioha et al. (20) Retrospective cohort; 2007–2008, Nigeria 910 19.6% Klebsiella spp. Amp, 41; Amc, 50; Czd, 77 Cipro, 78; Nal, 50 Gen, 48 41 50 NR Tet, 30
Other Enterobacteriaceaea or on the total isolates of Enterobacteriaceae of a study
    Nwadioha et al. (20) Retrospective cohort; 2007–2008, Nigeria 910 10% P. mirabilis, 7.1% P. vulgaris Amp, 18; Amc, 45; Ctrx, 83 (P. mirabilis); Amp, 40; Amc, 40; Ctrx, 80 (P. vulgaris) Cipro, 83; Nal, 45 (P. mirabilis); Cipro, 70; Nal, 40 (P. vulgaris) Gen, 55 (P. mirabilis) and 40 (P. vulgaris) 41 (P. mirabilis) and 40 (P. vulgaris) 55 (P. mirabilis) and 50 (P. Vulgaris) NR NR
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a

The term “other Enterobacteriaceae” refers to Enterobacteriaceae other than E. coli and Klebsiella spp. or other than those reported in each study.

Table 3.

Characteristics and outcomes of the included studies reporting on both OP and IP or on patients of undetermined origin

Isolate(s) and data source Study design; period, country Total no. of isolates; characteristic(s) Prevalence (%) of the studied pathogen Susceptibility of Enterobacteriaceae (%) to:
BLs FQs AGs SXT NTF FOS Other abx
Escherichia coli
    Aboderin et al. (16) Prospective cohort; 2004–2005, Nigeria 160; isolates both from outpatients and inpatients 25.6 Amx, 0; Amc, 2 Cipro, 15; Ofx, 24; Nal, 10 Gen, 0 5 80 NR Tet, 0
    Abubakar et al. (17) Prospective cross-sectional; 2007–2009, Nigeria 2,320 24.5 Amp, 16; Amc, 51; Pen, 33 Ofx, 65; Nal, 41 Gen, 20; Sm, 36 34 44 NR Erm, 44; Coli 36; Cam, 48; Tet, 14
    Ahmed et al. (37) Prospective cohort; NR, Sudan 362; isolates both from inpatients and outpatients NR Amx, 28; Amp, 25; Clx, 97; Cfx, 81; Cb, 33; Czd, 99 Cipro, 100; Nal, 94 Gen, 96; Amk, 100; Sm, 31 33 90 NR Tet, 33; Cam, 69; Tmp 26; Su, 31
    Bamford et al. (11) Retrospective cohort; 2007–2011, South Africa 38,329 isolates from public-sector laboratories and 320,514 isolates from private-sector laboratories; 9 and 8% in the public and private laboratories respectively, were ESBL-producing isolates NA Amp, 23; Amc, 73; narrow-spectrum Cephs, 78; expanded-spectrum Cephs, 90; broad-spectrum Cephs, 93 (both ESBL and non-ESBL; public); Amp, 26; Amc, 83; narrow-spectrum Cephs, 65; expanded-spectrum Cephs, 90; broad-spectrum Cephs, 94 (both ESBL and non-ESBL; private) Cipro, 83 (public); Cipro, 77; Lvf, 77 (private) Gen, 90; Amk, 97 (public); Gen, 90; Amk, 96 (private) 33 (public) 93 (public) NR NR
    Bouzenouneet al. (28) Retrospective cohort; 2006–2007, Algeria 239; 4.3% ESBL producing 71 Amp, 42; Amc, 50; Czl 86; Ctx, 99 Nal, 88; Ofx, 90 Gen, 99; Amk, 99 56 NR NR NR
    Dada-Adegbola et al. (18) Prospective cohort; 2000, Nigeria 409 19.1 Amp, 0; Amx, 0; Cfx, 25; Ctrx, 92; Czd, 78 Cipro, 82; Nal, 46; Ofx, 50; Pfx, 75 Gen, 62; Tob, 37; Amk, 75 2 66 NR Tet, 4; Coli7; Azi, 52
    Ghenghesh et al. (29) Prospective cohort; 2005–2006, Libya 187; isolates from patients with or without DM 15.7 Amp, 40; Amc, 65; Cth, 42; Ctx, 96 Cipro, 79; Nal, 71 Gen, 90; Sm, 58 73 NR NR Cam, 83
    Iweriebor et al. (12) Prospective cross-sectional; 2008–2009, South Africa 95; isolates from HIV patients 17.9 E. coli and Klebsiella spp. Amc, <77; Amp, <77; Pip, <77; Tzp, >80; Ctx, 100; Cxt, 100; Czl, >80; Cfx, >80; Imi, >80; Erta, <77; Azt, >80 (E. coli) Cipro, <77; Lvf, <77 (E. coli) Amk, 100; Tob, >80 (E. coli) <77 (E. coli) NR NR Tet, <77 (E. coli)
    Larabi et al. (14) Retrospective cohort; 1996–1998, Tunisia 1,930 69.5 (3.9 ESBL) Amp, 42; Tic 42; Cth, 78; Ctx, 96 Cipro, 100; Pfx, 96; Nal, 90 Gen, 99; Tob, 97; Amk, 98 53 98 NR NR
    Muvunyi et al. (32) Prospective cohort; 2009, Rwanda 196; isolates both from inpatients and outpatients 60.7 (6 ESBL) Amx, 8; Amc, 42; Pip 17; Cth, 16; Ctrx, 81; Czd, 85; Imi, 100 Cipro, 58; Nor, 59; Ofx, 59; Nal, 43 GEN, 60; Amk, 54 13 72 93 NR
    Nwanze et al. (21) Prospective cohort; 2004–2005, Nigeria 132; isolates from patients with suspected UTI 47.7 Cfx, 35 Cipro, 41; Nal, 21; Ofx, 81 Gen, 54; Tob, 46 NR NR Tet, 10
    Okesola et al. (22) Prospective cohort; 2009, Nigeria 200; isolates from patients with clinically diagnosed UTI 25 Amx, 0; Amc, 0 Nal, 4; Ofx, 30 Gen, 8 0 66 NR Tet, 12
    Smaoui et al. (15) MC retrospective study; 1999–2000, Tunisia 6,994 E. coli isolates NA Amx, 37; Amc, 66; Ctx, 97; Cth, 62; Cxt 98; Imi, 100 Cipro, 92; Ofx, 92; Nal, 87 Gen, 95 63 NR NR Tet, 53; Coli 99
Klebsiella spp.
    Abubakar et al. (17) Prospective cross-sectional; 2007–2009, Nigeria 2,320 17.3 K. pneumoniae Amp, 42; Amc, 65; Pen, 45 Ofx, 59; Nal, 55 Gen, 39; Sm, 44 39 52 NR Erm, 53; Coli 50; Cam, 51; Tet, 26
    Ahmed et al. (37) Prospective cohort; NR, Sudan 362; isolates both from inpatients and outpatients NR Amx, 15; Amp, 10; Clx, 88; Cfx, 80; Cb, 31; Czd, 92 Cipro, 100; Nal, 82 Gen, 60; Amk, 100; Sm, 31 32 54 NR Tet, 39; Cam, 58; Tmp, 27; Su, 28
    Bouzenoune et al. (28) Retrospective cohort; 2006–2007, Algeria 239; 4.3% ESBL producing 7.9 K. pneumoniae Amp, 0; Amc, 50; Czl 74; Ctx, 74 Nal, 84; Ofx, 84 Gen, 92; Amk, 92 37 NR NR NR
    Dada-Adegbola et al. (18) Prospective cohort; 2000, Nigeria 409 41.8 Klebsiella spp. Amp, 1; Amx, 3; Cfx, 30; Ctrx, 70; Czd, 66 Cipro, 75; Nal, 37; Ofx, 65; Pfx, 67 Gen, 46; Tob, 46; Amk, 73 1 49 NR Tet, 5; Coli, 26; Azi, 35
    Ghenghesh et al. (29) Prospective cohort; 2005–2006, Libya 187; isolates from patients with or without DM 13.7 Klebsiella spp. Amp, 0; Amc, 29; Cth, 34; Ctx, 73 Cipro, 71; Nal, 56 Gen, 63 88 NR NR Cam, 76
    Iweriebor et al. (12) Prospective cross-sectional; 2008–2009, South Africa 95; isolates from HIV patients 17.9 E. coli and Klebsiella spp. Amp, 0; Amc, 82; Pip, 91; Tzp, >80; Ticc, >80; Czd, >80; Czl, 18; Cfpm, 82; Cxt, 82; Ctrx, 82; Cfx, 82; Imi, 100; Azt, 82 (Klebsiella spp.) Lvf, 82 (Klebsiella spp.) Amk, 100; Gen, >80; Tob, >80 (Klebsiella spp.) >80 (Klebsiella spp.) NR NR Tet, 82 (Klebsiella spp.)
    Larabi et al. (14) Retrospective cohort; 1996–1998, Tunisia 1,930 9.3 K. pneumoniae (13.8 ESBL) Ctx, 84 Cipro, 98; Pfx, 94; Nal, 77 Gen, 99; Tob, 90; Amk, 94 45 79 NR NR
    Nwanze et al. (21) Prospective cohort; 2004–2005, Nigeria 132; isolates from patients with suspected UTI 12.9 K. pneumoniae Cxf, 53 Cipro, 47; Nal, 6; Ofx, 94 Gen, 41; Tob, 24 NR 6 NR Tet, 18
Other Enterobacteriaceaea or on the total Enterobacteriaceae of a study
    Abubakar et al. (17) Prospective cross-sectional; 2007–2009, Nigeria 2,320 14.6 P. mirabilis, 4.7 P. vulgaris, 4.1 Providencia stuartii, 2 S. marcescens, 1.7 C. freundii Amp, 47; Amc, 67; Pen, 31 (P. mirabilis); Amp, 34; Amc, 78; Pen, 39 (P. vulgaris); Amp, 28; Amc, 63; Pen, 35 (Providencia stuartii); Amp, 15; Amc, 66; Pen, 32 (S. marcescens); Amp, 15; Amc, 61; Pen, 28 (C. freundii) Ofx, 65; Nal, 51 (P. mirabilis); Ofx, 74; Nal, 57 (P. vulgaris); Ofx, 70; Nal, 41 (Providencia stuartii); Ofx, 62; Nal, 40 (S. marcescens); Ofx, 56; Nal, 54 (C. freundii) Gen, 49; Sm, 49 (P. mirabilis); Gen, 43; Sm, 48 (P. vulgaris); Gen, 33; Sm, 45 (Providencia stuartii); Gen, 47; Sm, 44 (S. marcescens); Gen, 15; Sm, 40 (C. freundii) 35 (P. mirabilis); 42 (P. vulgaris); 40 (Providencia stuartii); 43 (S. marcescens); 56 (C. freundii) 56 (P. mirabilis); 50 (P. vulgaris); 56 (Providencia stuartii); 68 (S. marcescens); 49 (C. freundii) NR Erm, 40; Coli 58; Cam, 37; Tet, 32 (P. mirabilis); Erm, 54; Coli 32; Cam, 61; Tet, 27 (P. vulgaris); Erm, 63; Coli 34; Cam, 59; Tet, 33 (Providencia stuartii); Erm, 58; Coli 49; Cam, 49; Tet, 17 (S. marcescens); Erm, 46; Coli 26; Cam, 49; Tet, 33 (C. freundii)
    Ahmed et al. (37) Prospective cohort; NR, Sudan 362; isolates both from inpatients and outpatients NR Amx, 22; Amp, 15; Clx, 96; Cfx, 85; Cb, 33; Czd, 92 (P. mirabilis); Amx, 56; Amp, 56; Clx, 33; Cfx, 56 (Enterobacter spp.) Cipro, 100; Nal, 93 (P. mirabilis); Nal, 78 (Enterobacter spp.) Gen, 63; Amk, 15; Sm, 42 (P. mirabilis); Gen, 44; Amk, 100 (Enterobacter spp.) 19 (P. mirabilis) and 44 (Enterobacter spp.) 41 (P. mirabilis) and 44 (Enterobacter spp.) NR Tet, 42; Cam, 64; Tmp, 17; Su, 19 (P. mirabilis)
    Bouzenoune et al. (28) Retrospective cohort; 2006–2007, Algeria 239; 4.3% ESBL producing 4.6 P. mirabilis, 3.3 other Enterobacteriaceae Amp, 36; Amc, 40; Czl, 73; Ctx, 91 (P. mirabilis); Amp, 0; Amc, 12; Czl, 12; Ctx, 75 (other Enterobacteriaceae) Nal, 91; Ofx, 91 (P. mirabilis); Nal, 43; Ofx, 71 (other Enterobacteriaceae) Gen, 87; Amk, 100 (P. mirabilis); Gen, 37; Amk, 100 (other Enterobacteriaceae) 64 (P. mirabilis) and 25 (other Enterobacteriaceae) NR NR NR
    Dada-Adegbola et al. (18) Prospective cohort; 2000, Nigeria 409 7.6 P. mirabilis, 3.7 Proteus spp. Amp, 13; Amx, 50; Cfx, 31; Ctrx, 75; Czd, 70 (P. mirabilis); Amp, 0; Cfx, 0; Ctrx, 78; Czd, 75 (Proteus spp.) Cipro, 71; Nal, 48; Ofx, 0; Pfx, 73 (P. mirabilis); Cipro, 100; Nal, 37; Ofx, 50; Pfx, 67 (Proteus spp.) Gen, 77; Tob, 68; Amk, 73 (P. mirabilis); Gen, 56; Tob, 50 (Proteus spp.) 9 (P. mirabilis) and 11 (Proteus spp.) 54 (P. mirabilis) and 43 (Proteus spp.) NR Tet, 5; Coli, 0; Azi, 100 (P. mirabilis); Tet, 11; Coli, 0; Azi, 0 (Proteus spp.)
    Iweriebor et al. (12) Prospective cross-sectional; 2008–2009, South Africa 95; isolates from HIV patients 37.6 Enterobacter spp., 9.7 Citrobacter spp. Amp, 55; Amc, 55; Pip, 55; Tzp, 85; Ticc, 85; Czl, 55; Cxt, 55; Cfpm, 85; Ctx, 85; Imi, 85; Erta, 55 (Enterobacter spp.); Amc, 44; Amp, >78; Pip, 100; Tzp, 100; Ticc, >78; Cfpm, 100; Ctx, 100; Ctrx, 100; Cxt, 34; Czl, 44; Cfx, >78; Imi, 100; Erta, >78; Azt, 100 (Citrobacter spp.) Cipro, 85 (Enterobacter spp.); Cipro, 100; Lvf, 100 (Citrobacter spp.) Amk, 100; Gen, 85; Tob, 85 (Enterobacter spp.); Amk, 100; Gen, 100; Tob, 100 (Citrobacter spp.) 55 (Enterobacter spp.) and >78 (Citrobacter spp.) NR NR Tet, 55 (Enterobacter spp.) and 34 (Citrobacter spp.)
    Larabi et al. (14) Retrospective cohort; 1996–1998, Tunisia 1,930 4.7 P. mirabilis (0.9 ESBL), 2.2 E. cloacae (55.4 ESBL) Amp, 24; Tic, 24; Cth, 64; Ctx, 99 (P. mirabilis); Ctx, 89 (E. cloacae) Cipro, 100; Pfx, 98; Nal, 87 (P. mirabilis); Cipro, 89; Pfx, 74; Nal, 50 (E. cloacae) Gen, 100; Tob, 81; Amk, 100 (P. mirabilis); Gen, 100; Tob, 59; Amk, 87 (E. cloacae) 39 (P. mirabilis) and 17 (E. cloacae) 0 (P. mirabilis) and 52 (E. cloacae) NR NR
    Nwanze et al. (21) Prospective cohort; 2004–2005, Nigeria 132; isolates from patients with suspected UTI 3.8 P. vulgaris Cfx, 20 Cipro, 80; Nal, 60; Ofx, 100 Gen, 40; Tob, 20 NR 40 NR Tet, 20
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a

The term “other Enterobacteriaceae” refers to Enterobacteriaceae other than E. coli and Klebsiella spp. or other than those reported by name in each study.

Outpatients. (i) Escherichia coli.

Eight studies reported the antimicrobial susceptibility of all E. coli isolates, irrespective of ESBL production (20, 24–26, 31, 34–36, 38). With regard to beta-lactams, the antimicrobial susceptibility varied among the studies at the following rates: amoxicillin-clavulanic acid, 16 to 86%; ticarcillin, 20 to 32%; cephalothin, 44 to 75%; cefoxitin, 89 to 98%; cefotaxime, 92 to 99%; and imipenem, 100%. The susceptibility of ciprofloxacin and nalidixic acid varied from 68 to 91% and 52 to 92%, respectively. Among aminoglycosides, the susceptibility of amikacin varied from 99 to 100%, while the susceptibility of gentamicin and tobramycin varied from 64 to 98% and from 82 to 99%, respectively. The susceptibility of other antibiotics that were tested varied at the following rates: trimethoprim-sulfamethoxazole, 15 to 66%; nitrofurantoin, 70 to 90%; fosfomycin, 98 to 100%; tetracycline, 22 to 57%; and chloramphenicol, 57 to 72%.

Two studies reported the susceptibility of the ESBL-producing isolates as well (27, 30). In the first one (27), among beta-lactams, the E. coli isolates were susceptible only to cefoxitin and imipenem, with a susceptibility of 100%. The susceptibility of the other antibiotics tested was the following: ciprofloxacin, 29%; nalidixic acid, 29%; gentamicin, 14%; tobramycin, 0%; amikacin, 86%; trimethoprim-sulfamethoxazole, 0%; and fosfomycin, 100%. In the second study (30), among all antibiotics tested, only imipenem and meropenem exhibited activity (100% for both antibiotics).

(ii) Klebsiella spp.

The antimicrobial susceptibility of Klebsiella species isolates was reported in 6 studies (19, 20, 23, 25, 35, 38) and varied at the following rates: amoxicillin-clavulanic acid, 0 to 69%; cefotaxime, 43 to 100%; ceftazidime, 40 to 100%; imipenem, 100%; ciprofloxacin, 53 to 100%; nalidixic acid, 51 to 94%; gentamicin, 60 to 100%; amikacin, 100%; trimethoprim-sulfamethoxazole, 0 to 56%; nitrofurantoin, 40 to 78%; tetracycline, 43 to 69%; and fosfomycin, 100%.

Other Enterobacteriaceae.

Eight studies reported on Enterobacteriaceae other than E. coli and Klebsiella spp. or on the total number of isolates of Enterobacteriaceae included in a study (19, 20, 25, 31, 33–36, 38). Two of them reported on Proteus spp. (19, 20). Both studies presented the susceptibility of P. mirabilis separately from that of P. vulgaris. In the first study, the percentages of susceptibility for P. mirabilis and P. vulgaris isolates were the following: cefixime, 63 and 100%; ofloxacin, 88 and 100%; nalidixic acid, 75 and 67%; gentamicin, 75 and 67%; and nitrofurantoin 63 and 67%, respectively (19). In the other study (20), the susceptibility of the P. mirabilis and P. vulgaris isolates was the following: amoxicillin-clavulanic acid, 53 and 53%; ceftriaxone, 96 and 98%; ciprofloxacin, 96 and 95%; nalidixic acid, 53 and 51%; gentamicin, 72 and 71%; trimethoprim-sulfamethoxazole, 48 and 46%; nitrofurantoin, 62 and 53%; and tetracycline, 47 and 46%, respectively.

Only one study of this category reported the susceptibility of the ESBL-producing Enterobacteriaceae (33). Forty-two percent of these isolates were susceptible to amoxicillin-clavulanic acid, 61% to cephalothin, 98% to cefotaxime, 74% to ciprofloxacin, 67% to nalidixic acid, 83% to gentamicin, 16% to trimethoprim-sulfamethoxazole, and 99% to fosfomycin.

Inpatients. (i) Escherichia coli.

In one study reporting on patients with hospital-acquired UTIs, 45% of the isolates were susceptible to amoxicillin-clavulanic acid, 81% to ceftriaxone, 86% to ciprofloxacin, 44% to nalidixic acid, 48% to gentamicin, 38% to trimethoprim-sulfamethoxazole, 53% to nitrofurantoin, and 38% to tetracycline (20).

(ii) Klebsiella spp.

Only one study reported on hospitalized patients exclusively (13). The susceptibility of all Klebsiella spp. isolates to the antibiotics tested was the following: amoxicillin-clavulanic acid, 60%; cefotaxime, 66%; nalidixic acid, 48%; ofloxacin, 73%; ciprofloxacin, 74%; gentamicin, 69%; tobramycin, 70%; amikacin, 97%; trimethoprim-sulfamethoxazole, 57%; nitrofurantoin, 68%; and fosfomycin, 77%. When only the ESBL-producing isolates were tested, the susceptibility was the following: amoxicillin-clavulanic acid, 0%; cefotaxime, 0%; nalidixic acid, 20%; ofloxacin, 32%; ciprofloxacin, 32%; gentamicin, 7%; tobramycin, 10%; amikacin, 90%; trimethoprim-sulfamethoxazole, 27%; nitrofurantoin, 47%; and fosfomycin, 82%.

Among patients with hospital-acquired UTIs, 50% of the isolates were susceptible to amoxicillin-clavulanic acid, 77% to ceftazidime, 78% to ciprofloxacin, 50% to nalidixic acid, 48% to gentamicin, 41% to trimethoprim-sulfamethoxazole, 50% to nitrofurantoin, and 30% to tetracycline (20).

Other Enterobacteriaceae.

The study reporting on patients with hospital-acquired UTIs provided antimicrobial susceptibility data for Proteus spp. as well (20). Forty-five percent and 40% of P. mirabilis and P. vulgaris isolates were susceptible to amoxicillin-clavulanic acid, 83 and 80% to ceftriaxone, 83 and 70% to ciprofloxacin, 45 and 40% to nalidixic acid, 55 and 40% to gentamicin, 41 and 40% to trimethoprim-sulfamethoxazole, and 55 and 50% to nitrofurantoin, respectively.

Both outpatients and inpatients or undetermined origin of the study population. (i) Escherichia coli.

Thirteen studies in the category of outpatients and inpatients from study populations of undetermined origin reported the antimicrobial susceptibility of E. coli isolates (11, 12, 14–18, 21, 22, 28, 29, 32, 37), which varied among studies at the following rates: amoxicillin-clavulanic acid, 0 to 77%; cefotaxime, 96 to 100%; imipenem, 80 to 100%, ciprofloxacin 15 to 100%, nalidixic acid 4 to 94%, ofloxacin 24 to 92%, gentamicin 0 to 99%; tobramycin, 46 to 97%; amikacin, 54 to 100%; trimethoprim-sulfamethoxazole, 0 to 77%; nitrofurantoin, 44 to 98%; and tetracycline, 0 to 77%.

One study provided microbiological data on urine E. coli isolates collected from 5 public and 14 private laboratories in South Africa from 2007 to 2011 (11). Antimicrobial susceptibility data were available for a total of 358,843 isolates (38,329 from the public sector, 320,514 from the private sector). The susceptibility of all isolates, both ESBL and non-ESBL producing, collected from public and private laboratories was the following: ampicillin, 23 and 26%; amoxicillin-clavulanic acid, 73 and 83%; narrow-spectrum generation cephalosporins, 78 and 65%; expanded-spectrum cephalosporins, 90 and 90%; and broad-spectrum cephalosporins, 93 and 94%, respectively.

(ii) Klebsiella spp.

Eight studies reported on Klebsiella species isolates (12, 14, 17, 18, 21, 28, 29, 37). Among the studies, the susceptibility varied from 29 to 82% for amoxicillin-clavulanic acid, 74 to 84% for cefotaxime, 47 to 100% for ciprofloxacin, 54 to 94% for ofloxacin, 6 to 84% for nalidixic acid, 39 to 99% for gentamicin, 73 to 100% for amikacin, 1 to 88% for trimethoprim-sulfamethoxazole, 6 to 79% for nitrofurantoin, and 5 to 82% for tetracycline.

Other Enterobacteriaceae.

Seven studies reported on Enterobacteriaceae other than E. coli or Klebsiella spp. or on the total number of isolates of Enterobacteriaceae included in a study (12, 14, 17, 18, 21, 28, 37). Six of them provided antimicrobial susceptibility data on Proteus spp. (4 on P. mirabilis [14, 18, 28, 37], 1 on P. vulgaris [21], and 1 on both P. mirabilis and P. vulgaris [17]). With regard to P. mirabilis, 15 to 47% of the isolates were susceptible to ampicillin, 100% to ciprofloxacin, 48 to 93% to nalidixic acid, 49 to 100% to gentamicin, 15 to 100% to amikacin, 9 to 64% to trimethoprim-sulfamethoxazole, 0 to 56% to nitrofurantoin, 5 to 42% to tetracycline, and 37 to 64% to chloramphenicol. The susceptibility of the P. vulgaris isolates varied at the following rates: ampicillin, 34%; amoxicillin-clavulanic acid, 78%; penicillin, 39%; cefuroxime, 20%; ciprofloxacin, 80%; nalidixic acid, 57 to 60%; ofloxacin, 74 to 100%; gentamicin, 40 to 43%; tobramycin, 20%; streptomycin, 48%; trimethoprim-sulfamethoxazole, 42%; nitrofurantoin, 40 to 50%; tetracycline, 20 to 27%; chloramphenicol, 61%; colistin, 32%; and erythromycin, 54%.

DISCUSSION

The findings of the review suggest that the antimicrobial susceptibility of Enterobacteriaceae causing UTIs in Africa is similar to the susceptibility in countries of southeast Europe and better than the susceptibility observed in India and certain other Asian countries (9, 39–42). Although the available data originated from both northern Africa and sub-Saharan Africa, no evident difference with regard to antimicrobial susceptibility was observed among the developed and developing countries of northern and southern Africa, probably due to mobility of the local populations.

With regard to E. coli isolates, cefotaxime and imipenem exhibited very good activity, while, in general, ciprofloxacin had the highest activity among oral antibiotics. In addition, the isolates recovered from outpatients were highly susceptible to fosfomycin. Among Klebsiella species isolates, amikacin and ciprofloxacin were among the antibiotics with the highest activity, while isolates recovered from inpatients were highly susceptible to fosfomycin. Fluoroquinolones, namely, ciprofloxacin and ofloxacin, were the most active antibiotics against Proteus species isolates. Consistent with published data from other continents (43), fosfomycin exhibited very good activity against ESBL-producing isolates; in fact, it was the most active antibiotic against the ESBL-producing E. coli and Klebsiella species isolates collected from patients with UTIs in Africa. In general, the broad-spectrum cephalosporins, imipenem, ciprofloxacin, amikacin, and fosfomycin were the antibiotics with the highest activities, followed by cefoxitin, cephalothin, amoxicillin-clavulanic acid, gentamicin, tobramycin, nalidixic acid, cotrimoxazole, and nitrofurantoin. It should be highlighted that fosfomycin exhibited high activity against most Enterobacteriaceae isolates. Taking into consideration the low cost of this antibiotic along with the possibility of oral administration, it seems to be the preferable treatment option against UTIs in countries with limited financial resources.

The available data are completely representative of the antimicrobial susceptibility of Enterobacteriaceae causing UTIs in South Africa after 2007, since >300,000 isolates from both public and private laboratories were included in the review of that period. A very good sample of urine isolates was also available for Tunisia, Nigeria, and Senegal, offering a satisfactory view of the antimicrobial susceptibility among the most common uropathogens in these countries. Being aware of the local antimicrobial susceptibility of Enterobacteriaceae uropathogens makes it more possible for clinicians to prescribe an appropriate empirical antibiotic treatment. Therefore, patients would experience fewer treatment failures and health care costs would decrease.

The lack of drugs in many African countries seems to be the most rational explanation for the better antimicrobial susceptibility of uropathogens in Africa than in certain Asian countries where the availability of drugs is far better, as more resistant strains appear when more antibiotics are used. The availability of drugs could also justify the same positioning of the antimicrobial susceptibility of Enterobacteriaceae in African countries compared to that of certain European countries where antibiotics are overused. Studies from Europe and North America showed that the antimicrobial susceptibility patterns of E. coli, Klebsiella species, and Proteus species isolates collected from outpatients (44, 45) and inpatients (46) with UTIs were similar to those presented in studies from Africa.

Our study should be interpreted in light of certain limitations. The main limitation of our study is that the antimicrobial susceptibility breakpoints used by the investigators of the included studies have changed for many antibiotics. Accordingly, isolates that were interpreted as susceptible by the investigators of the individual studies may now be resistant according to the updated susceptibility breakpoints. Also, the limitations arising from the different antimicrobial susceptibility tests performed by the different laboratories and from differences in quality control for antimicrobial susceptibility (i.e., growth conditions) in different countries should be considered in the interpretation of the findings of this review. In addition, for many African countries there were no available data, while for some others the available data were very limited. Accordingly, a safe conclusion on the antimicrobial susceptibility of Enterobacteriaceae uropathogens for the whole continent could not be drawn. In addition, the antibiotics that were tested were not the same for all included studies, while very few data were available for certain antibiotics. However, sufficient data were available for the majority of the most commonly used antibiotics against UTIs. We should note that is not clear whether one study (12) includes a population which is included in another published study (11).

In conclusion, the currently available data, which are representative of a satisfactory part of Africa, suggest that the antimicrobial susceptibility of Enterobacteriaceae causing UTIs is not as low as one might expect. Clinicians should be aware of the existing data and treat patients according to the susceptibility patterns. Further studies from African countries with no or limited published data are warranted.

ACKNOWLEDGMENT

We have no conflicts of interest or transparency issues to declare.

Footnotes

Published ahead of print 20 May 2013

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