Table 1.
Main results of the studies included in this work
| WHO areaa | Yr of studyb | Country | No. of individuals included | ESBL carriage rate (% [no. of ESBL carriers])c | % of carriers with CTX-M-type ESBL (no. of positive results/total no. of carriers)d | Species identified (no. with species/total no. of carriers)d,e,f | CTX-M allele(s) identified (no. of isolates with allele/total no. of carriers)d,g | Clonality rate (%) (detection method)d,h | ST identifiedd | Independent risk factor(s) identified (by multivariate model)d | Subjectse | Reference |
|---|---|---|---|---|---|---|---|---|---|---|---|---|
| Europe | 1999 | France | 517 | 0 (0) | NA | NA | NA | NA | NP | NP | Army recruits | 61 |
| 2001–2002 | Spain | 1,321 | 3.3 (44) | 75 (33/44) | Ecol (42/44), Pmir, Eclo | 9 (18/33), 14, 15, 29, 1, 3, 34 | NP | NP | NP | Emergency patients | 56 | |
| 2003 | UK | 565 | 1.6 (9) | 100 (9/9) | Ecol (8/9), Salm spp. | 15 (4/9), 14, 9 | None (RAPD) | NP | NP | General practice patients | 63 | |
| 2003 | Spain | 108 | 3.7 (4) | 50 (2/4) | Ecol | 14, 2-like | None (PFGE) | NP | NP | Healthy individuals | 54 | |
| 2003 | Spain | 948 | 6.6 (63) | NP | Ecol (73/75), Kp, Ckos | NP | NP | NP | NP | Emergency patients | 55 | |
| 2005–2006 | Spain | 54 | 7.4 (4) | 50.0 (2/4) | Ecol | 14 | None (rep, PFGE) | NP | NP | Healthy individuals (controls of a case-control study) | 57 | |
| 2006 | France | 332 | 0.6 (2) | 0 (0/2) | NA | NA | NA | NA | NA | Healthy individuals | 62 | |
| 2007 | Spain | 105 | 6.7 (7) | 85.7 (6/7) | Ecol | 1 (2/6), 14a, 14b, 8, 32 | NP | NP | NP | Healthy individuals, only Ecol studied | 145 | |
| 2007–2008 | Portugal | 112 | 2.7 (3) | 33.3 (1/3) | Ecol | 1 | NP | NP | NP | Healthy children, only Ecol studied | 59 | |
| 2008 | Denmark | 84 | 3.6 (3) | 100 (3/3) | Ecol | 14a | 2/3 in 1 clone (ST1631) (MLST, PFGE) | 1631, 641 | None identified | Army recruits | 60 | |
| 2008 | Sweden | 96 | 2.1 (2) | 93.8 (15/16) | Ecol | 1 (11/15), 9 | None (rep, serotyping) | NP | None identified | Healthy individuals | 64 | |
| 2010 | Sweden | 100 | 3.0 (3) | Ecol | ||||||||
| 2008 | France | 500 | 6.6 (33) | 78.8 (26/33) | Ecol (21/26), Kp, Eclo | 15 (11/26), 1, 14, 65, 27 | 3/28 in 1 clone (rep) | NP | Previous carriage, antibiotic use during the last 3 months | Patients with first admission to hospital | 67 | |
| 2009 | France | 517 | 2.1 (11) | 90.1 (10/11) | Ecol (9/10), Kp | 15 (3/10), 61 (3/10), 2, 27, 14 | None (PFGE) | NP | NP | Army recruits | 61 | |
| 2010 | Switzerland | 586 | 5.8 (34) | 97.1 (33/34) | Ecol | 15 (14/33), 1, 14, 2 | 3*2 and 1*3 clones (serotyping) | NP | NP | Healthy individuals | 65 | |
| 2010–2011 | Belgium | 337 | 11.6 (39) | 71.8 (28/39) | Ecol (39/45), Kp, Ent spp., Cit spp. | Group 1 predominant | NP | NP | Multiple contacts with hospital over 1 year (long term) | Geriatric unit admission | 23 | |
| 2011 | Germany | 231 | 3.5 (8) | NP | Ecol | NP | NP | NP | Travel to Greece and Africa during the past 12 months, domestic animals | Participants in a symposium | 146 | |
| 2011 | France | 345 | 6 (21) | 86 (18/21) | Ecol | 15 (7/18), 1 (7/18), 14, 2 | 4/18 in 2 clones (361 and 131) (MLST, PFGE) | 156, 10, 167, 744, 34, 210, 216, 1125, 155, 95, 131, 141, 69, 120, 5211, 2439 | None | Healthy individuals | 69 | |
| Eastern Mediterranean | 2003 | Lebanon | 382 | 2.4 (9) | 100 (9/9) | Ecol | 15 | None (MLST) | NP | NP | Healthy students | 70 |
| 2006 | Saudi Arabia | 426 | 13.1 (56) | NP | Ecol (52/56), Kp | NP | NP | NP | NP | Healthy students, only Ecol and Kp were selected | 147 | |
| 2006–2007 | Saudi Arabia | 505 | 12.3 (62) | NP | Ecol (?), Kp | NP | NP | NP | NP | Healthy individuals | 148 | |
| 2009–2010 | Tunisia | 150 | 7.3 (11) | 91.0 (10/11) | Ecol | 1 | 3/10 in 1 clone (ST58) (PFGE, MLST) | 165, 57, 155, 58, 10, 48, 398, 219 | NP | Healthy individuals | 71 | |
| 2010–2011 | Egypt | 632 | 63.3 (400) | NP | Ecol (285/400), Kp, Ko, Ent spp. | NP | NP | NP | NP | Healthy individuals | 72 | |
| Africa | 2007–2008 | Niger | 55 | 30.9 (17) | 90.9 (20/22) | Ecol (13/20), Kp, Eclo, Easb | 15 | 3/17 in 1 Ecol clone (ST361) (rep, PFGE, MLST) | 361, 354, 5, 131, 10, 101, 68, 448, 196, 617, 410 | NP | Pediatric admission | 74 |
| 2008* | Senegal | 20 | 10.0 (2) | 100 (2/2) | Ecol | 15 | 100 (2/2) (rep) | NP | NP | Healthy children | 73 | |
| 2008 | Madagascar | 244 | 22.1 (54) | NP | Ecol (24/54), Kp (24/54), Eclo, other EB | NP | NP | NP | Hospitalization during the last 30 days | Pediatric admissions | 76 | |
| 2009 | Madagascar | 484 | 10.1 (49) | 94.2 (49/52) | Ecol (31/49), Kp, Eclo, Cf, Klu, Pan | 15 (46/49), 3, 1 | 8/53 in 3 Ecol clones (rep, ERIC) | NP | Unemployment | Healthy individuals | 75 | |
| 2009 | Cameroon | 150 | 6.7 (10) | 100 (10/10) | Ecol (9/10), Kp | 15 | NP | NP | None | Healthy students | 149 | |
| Southeast Asia | 2001–2002 | Indonesia | 1,998 | 0 (0/1,998) | NA | NA | NA | NA | NP | NP | Healthy individuals, only the dominant flora was studied | 77 |
| 2008 | Thailand | 160 | 61.7 (87) | 94.3 (82/87) | Ecol (73/82), Cit spp., Kp, Ent spp., Salm spp., other EB | Group 9 (71/82), group 1 | NP | NP | NP | Healthy individuals | 22 | |
| 2009 | Thailand | 445 | 40 (177) | 92.7 (164/177) | Ecol (149/164), Cit spp., other | Group 9 (127/164), group 1, group 8 | NP | NP | Antibiotic exposure (?) | Healthy individuals | 79 | |
| 2010 | Thailand | 417 | 69.3 (289) | 94.8 (274/289) | Ecol (234/274), Kp, Cit spp., Ent spp. | Group 9 (166/274), group 1, group 8 | NP | NP | Formal education, hospitalization over past year, antibiotic use during last 3 months | Healthy individuals | 78 | |
| Western Pacific region | 2002 | China | 53 | 11.3 (6) | 100 (6/6) | Kp (4/6), Ecol | 24 (2/6), 38 (2/6), 9, 14 | 4/6 in 2 clones (PFGE) | NP | NP | Healthy students | 150 |
| 2007* | China | 270 | 7.0 (19) | 100 (19/19) | Ecol | 14 (11/19), 22, 79, 24 | None (PFGE) | NP | Antibiotic use in past <3 months | Elderly people | 81 | |
| 2007–2008 | China | 225 | 45.8 (103) | 95.4 (104/109) | Ecol (88/109), Kp | 14 (65/104), 15, 3, 24, 27, 55, 57 | 15/109 in 6 clones (PFGE) | NP | Amount of living space per person | Pediatric admissions and household contacts | 98 | |
| 2009 | China | 109 | 50.6 (55) | 100 (55/55) | Ecol | 14 (39/55), 15, 55, 79, 3, 24, 27 | None (PFGE) | NP | NP | Healthy individuals | 80 | |
| 2009–2010 | Japan | 218 | 6.4 (14) | 92.9 (13/14) | Ecol (11/13), Kp | 14 (5/13), 2, 8, 3, 15 | NP | NP | None | Healthy individuals | 151 | |
| 2011 | Korea | 290 | 20.3 (59) | NP | Ecol (57/59), Kp | NP | NP | NP | NP | Healthy individuals | 152 | |
| The Americas | 2002 | Bolivia and Peru | 3,208 | 0.1 (4) | 100 (4/4) | Ecol | 2 (3/4), 15 | NP | NP | NP | Healthy children, only Ecol was selected | 83 |
| 2005 | Bolivia and Peru | 3,193 | 1.7 (50) | 88.0 (44/50) | Ecol | 2 (16/44), 15, 14, 24, 56 | 19/44 in 6 clones (RAPD) | NP | NP | Healthy children, only Ecol was selected | 153 | |
| 2006 | French Guiana | 163 | 8.0 (13) | 86.0 (12/14) | Ecol | 2 (11/15), 8 | 9/14 in 2 clones (rep) | NP | Overall antibiotic pressure (?) | Healthy individuals | 85 | |
| 2011 | Bolivia and Peru | 482 | 12.4 (60) | 96.7 (58/60) | Ecol | 15 (23/58), 65, 8, 14, 2, 3 | 25/58 in 9 clones (RAPD) | NP | Antibiotic use | Healthy children, only Ecol was selected | 84 | |
| Travelers | 2006–2008 | UK | 1,031 | 17.7# (182) | 100 (182/182) | Ecol | 15 (174/182), group 9, group 2 | 1 clone of 21 ST131 clones identified (MLST, PFGE) | Only ST131 strains were detected | NP | Travelers with diarrhea | 89 |
| 2007–2008 | Sweden | 101 (before) | 1.0 (1) | 100 (24/24) | Ecol | 15 (13/24), 14, 9, 27, 1 | NP | NP | Visiting India, gastroenteritis | Travelers (before versus after travel) | 91 | |
| 100 (after) | 24.0# (24) | |||||||||||
| 2008 | Sweden | 242 | 24.0# (58) | 90 (52/58) | Ecol | Group 1 (35/52), group 9 | None (rep) | NP | Travel, excluding Europe (Egypt, Thailand, India, Middle East, Southeast Asia) | Travelers with diarrhea | 90 | |
| 2009–2010 | USA | 60 (before) | 1.6 (1) | NP | NP | NP | NP | NA | NP | Travelers (before versus after travel) | 86 | |
| 28 (after) | 25.0 (7) | 71.4 (5/7) | Ecol | 14 (3/5), 15 | None (MLST) | 39, 8, 37, 399, 8, 437,83 | NP |
a
Studies were grouped together according to WHO geographical areas (http://www.who.int/healthinfo/global_burden_disease/definition_regions/en/index.html; accessed 18 December 2012).
b
*, studies in which the year of sampling was not specified. In those cases, the year indicated is the year before the year of publication.
c
#, the carriage rate value was not included in the statistical analysis.
d
NA, not applicable; NP, not performed.
e
Ecol, Escherichia coli; Salm, Salmonella; Pmir, Proteus mirabilis; Eclo, Enterobacter cloacae; Kp, Klebsiella pneumoniae; Ckos, Citrobacter koseri; Ent, Enterobacter; Cit, Citrobacter; Ko, Klebsiella oxytoca; EB, Enterobacteriaceae; Cf, Citrobacter freundii; Klu, Kluyvera; Pan, Pantoea; Easb, Enterobacter asburiae.
f
The dominant enterobacterial species is shown in bold. The dominant species is either the dominant species among CTX-M strains (when such data are known) or the dominant species among ESBL strains.
g
The dominant allele or allelic group is shown in bold.
h
RAPD, random amplification of polymorphic DNA; PFGE, pulsed-field gel electrophoresis; rep, repetitive element palindromic PCR; MLST, multilocus sequence typing; ERIC, enterobacterial repetitive intragenic consensus PCR.