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Original article

Urinary tract infections in hospital pediatrics: Many previous antibiotherapy and antibiotics resistance, including fluoroquinolones Infections urinaires en pédiatrie hospitalière : beaucoup d’antibiothérapie préalable et d’antibiorésistance, y compris vis à vis des fluoroquinolones A. Garraffo a,∗,b , C. Marguet a , A. Checoury b , S. Boyer c , A. Gardrat d , E. Houivet e , F. Caron f a

Service de pédiatrie générale, CHU de Rouen, 1, rue de Germont, 76000 Rouen, France Service de pédiatrie générale, CHG d’Évreux, rue L.-Schwartzenberg, Évreux, France c Service de bactériologie, CHU de Rouen, 1, rue de Germont, Rouen, France d Service de bactériologie, CHG d’Évreux, rue L.-Schwartzenberg, Évreux, France e Service de biostatistiques, CHU de Rouen, 1, rue de Germont, Rouen, France f Service de maladies infectieuses et tropicales, CHU de Rouen, 1, rue de Germont, Rouen, France b

Received 20 February 2013; received in revised form 18 September 2013; accepted 2 December 2013 Available online 7 February 2014

Abstract Objective. – We studied antibiotic resistance in pediatric UTIs and we evaluated the impact of antibiotic exposure in the previous 12 months, very little French data being available for this population. Methods. – We conducted a multicenter prospective study including children consulting for, or admitted in 2 hospitals. Prior antibiotic exposure was documented from their health record. Results. – One hundred and ten patients (73 girls), 11 days to 12 years of age, were included in 10 months. Ninety-six percent presented with pyelonephritis, associated to uropathy for 25%. Escherichia coli was predominant (78%), followed by Proteus spp. and Enterococcus spp. The antibiotic resistance rate of E. coli was high and close to that reported for adults with complicated UTIs: amoxicillin 60%, amoxicillin-clavulanate 35%, cefotaxim 5%, trimethoprim-sulfametoxazole 26%, nalidixic acid 9%, ciprofloxacin 7%, gentamycin 1%, nitrofurantoin and fosfomycin 0%. The antibiotic exposure in the previous 12 months involved 62 children (56%) most frequently with ␤-lactams (89%) for a respiratory tract infection (56%). A clear relationship between exposure and resistance was observed for amoxicillin (71% vs. 46%), first generation (65% vs. 46%) and third generation (9% vs. 3%) cephalosporins, or trimethoprim-sulfamethoxazole (36% vs. 15%). However, antibiotic exposure could not account alone for the results, as suggested by the 7% of ciprofloxacin resistance, observed without any identified previous treatment. Conclusion. – Bacterial species and antibiotic resistance level in children are similar to those reported for adults. Antibiotic exposure in the previous 12 months increases the risk of resistance but other factors are involved (previous antibiotic therapies and fecal-oral or mother-to-child transmission). © 2013 Elsevier Masson SAS. All rights reserved. Keywords: Bacterial resistance; Pediatric; Urinary tract infection

Résumé Objectifs. – Étudier l’antibiorésistance des infections urinaires en pédiatrie hospitalière et la confronter à l’exposition antibiotique dans les 12 mois antérieurs, très peu de données franc¸aises étant disponibles pour cette population. Patients et méthodes. – Analyse prospective des enfants consultants ou hospitalisés dans deux hôpitaux, leur exposition antibiotique étant renseignée d’après le carnet de santé. Résultats. – Recueil en dix mois de 110 cas (73 filles), âgés de 11 jours à 12 ans, 96 % souffrant de pyélonéphrites, dont 25 % sur uropathie. Dominance d’Escherichia coli (78 %) devant Proteus et entérocoque. Antibiorésistance d’E. coli élevée, comparable à celle de séries d’infections ∗

Corresponding author. E-mail address: [email protected] (A. Garraffo).

0399-077X/$ – see front matter © 2013 Elsevier Masson SAS. All rights reserved. http://dx.doi.org/10.1016/j.medmal.2013.12.002

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urinaires compliquées de l’adulte : amoxicilline 60 %, amoxicilline-clavulanate 35 %, céfotaxime 5 %, cotrimoxazole 26 %, acide nalidixique 9 %, ciprofloxacine 7 %, gentamicine 1 %, nitrofurantoïne et fosfomycine 0 %. L’exposition antibiotique dans les 12 mois antérieurs concernait 62 enfants (56 %), majoritairement par ␤-lactamines et pour infection respiratoire (89 % et 56 % des exposés, respectivement), avec une nette corrélation entre l’exposition antibiotique et l’antibiorésistance d’E. coli à l’amoxicilline (71 % vs 46 %), les C1G (65 % vs 46 %), les C3G (9 % vs 3 %) et le cotrimoxazole (36 % vs 15 %). Cependant, l’exposition antibiotique n’expliquait pas tout (7 % de résistance à la ciprofloxacine sans traitement préalable identifié). Conclusion. – Les espèces bactériennes et niveaux d’antibiorésistance chez l’enfant sont similaires à ceux actuellement observés en France chez l’adulte. L’exposition antibiotique dans les 12 mois majore le risque de résistance, mais d’autres facteurs sont en cause (rôle probable des traitements plus anciens et de la contamination oro-fécale, voire materno-fœtale pour les plus jeunes). © 2013 Elsevier Masson SAS. Tous droits réservés. Mots clés : Infection urinaire ; Pédiatrie ; Résistances bactériennes

1. Introduction Therapeutics recommendations depend on the surveillance of antibiotic resistance, especially for the empirical treatment of severe infections. The epidemiological variations, sometimes important from one country to another, including within Europe (www.ecdc.org), justify obtaining national statistics. But, in the domain of urinary tract infection (UTI), the French National Observatory for Epidemiology of Bacterial Resistance to Antimicrobials (French acronym ONERBA) (www.onerba.org) does not specify any pediatric particularity. It is nevertheless one of the most frequent bacterial infections in children that, without an optimal treatment, exposes to the risk of a renal scarring and nephron loss [1,2]. The antibiotic exposure of children, a large source of antibiotic resistance, a fortiori for UTIs induced by bacteria of digestive flora, is significantly different from that of adults, more important in volume in the first years of life (because of the frequency of respiratory infections), but sparing some antibiotics classes such as fluoroquinolones and in a lesser way aminoglycosides [3]. In France, this exposure to antibiotics is much easier to analyze in children, using the healthcare record globallly well documented both in community and in hospital practice, thanks to the vigilance of parents and healthcare personnel, whereas this tool is missing for adults [4]. The objective of this pilot study conducted in 2 Normandy hospital centers was to assess the antibiotic resistance of isolates from UTIs in children, and to compare it to exposure to antibiotics in the previous 12 months as documented in the healthcare record. The results were compared to antibiotic resistance data of adult UTI isolates collected in the same region thanks to 2 other concomitant studies [5,6]. 2. Material and methods

clinical signs (functional urinary signs, altered global health status, abdominal pains, etc.) and positive urine microscopy and culture (UMC). Fever (> 38 ◦ C) and a biological inflammatory syndrome (CRP > 5) were also required to diagnose a pyelonephritis. 2.2. Urinalysis Urine was collected after careful disinfection of the meat with sodium hypochlorite (Dakin solution® ) by healthcare personnel (nurse or child care assistant). The urine was collected at midstream in all children with voluntary urination; for infants, it was performed with collection bags (placed for less than 1 hour). In some rare cases, urine was collected by a 2-way vesical catheter. UMC was performed in the bacteriology laboratories of the Rouen TH and of the Evreux GH, on centrifuged urine. The positivity threshold were those define by the French Agency for the safety of Health Product (French acronym Afssaps) for children, i.e. leukocyturia ≥ 104 /ml and bacteriuria > 104 UFC/ml [7]. The antibiograms were analyzed according to recommendations issued by the Antibiogram Committee of the French Microbiology Society (CA-SFM, www.sfm-microbiology.org). 2.3. Patient history and previous antibiotic treatment We documented the following history for each child included: any previous episodes of UTI or of a known underlying uropathy (vesical ureteral reflux, mega ureter, dilatation of pyelocalyceal cavities, hydronephrosis, ureteral duplication, etc.), exposure to antibiotics in the 12 months before the UTI was also documented, specifying the name of the administered antibiotic and the reason for its prescription. This data was collected during an interview with the parents with, whenever it was possible, study of the child’s healthcare record. The data was documented with a standardized questionnaire by the physician managing the child.

2.1. Study population

2.4. Statistical analysis

Children 0 to 15 years of age, consulting or hospitalized at the Rouen teaching hospital (TH) or at the Evreux general hospital (CH) for an UTI, were included in a prospective study from January 1st to October 30th, 2011. The diagnosis of UTI (cystitis or pyelonephritis) had been made for each child, by a physician of the ward, because of a combination of suggestive

The statistical analysis assessing the risk of antibiotic resistance according to exposure to antibiotics in the previous focused on Escherichia coli, by grouping intermediately resistant and resistant strains. The rate of antibiotic resistance in the group of children exposed to antibiotics was compared to that of children not exposed, with the Chi2 test for populations > 5 and Fischer’s

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test for smaller populations. The threshold of significance was set with an alpha risk < 5%, or p < 0.05. The results were adjusted according to age, the child’s gender, and of the presence or not of a uropathy, so as to take into account the potential influence related to these intrinsic pediatric factors. Then, to avoid the bias related to multiple comparisons, a complementary analysis by with Bonferroni correction was made, by grouping the antibiotics by classes: ␤-lactams (amoxicillin, amoxicillin-clavulanate, first generation (1st GC) or third generation (3rd GC) cephalosporins, imipenem), quinolones (nalidixic acid, ciprofloxacin), aminoglycosides (gentamycin, netromycin). The threshold of significance, after this Bonferroni correction, was set at p < 0.0125. 3. Results 3.1. Study population One hundred and ten children (81 at the Rouen TH and 29 at the Evreux GH) were included in 10 months, as listed in Table 1, including 73 girls and 37 boys (sex ratio = 0.51), 11 days to 12 Table 1 Patients features. Caractéristiques de la population. Variables

Number of individualsa (%)

Age Neonates (< 28 days) Infants (28 days–2 years) Children (2–16 years)

2 (2%) 64 (58%) 44 (40%)

Sex Male Female

37 (34%) 73 (66%)

Documented uropathy Boys Girls

27 (25%) 17 (46% of boys) 10 (14% of girls)

History of UTI Boys Girls

22 (20%) 6 (16% des boys) 16 (22% des girls)

Clinical presentation Pyelonephritis Cystititis

105 (95%) 5 (5%)

Place of management Hospital Ambulatory

91 (83%) 19 (17%)

Antibiotic treatment ≤ 1 year: all classes ␤-lactams Penicillins Cephalosporins Carbapenems Cotrimoxazole Aminoglycosides Macrolides Furanes Fluoroquinolones Fosfomycin Penems Missing data

62 (56%) 55 (89% of children) 34 (31%) 37 (34%) 0 (0%) 18 (16%) 15 (14%) 8 (7%) 7 (6%) 0 (0%) 0 (0%) 0 (0%) 3 (3%)

a

Percentage of the total population.

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years of age, with a predominance of infants (60% less than 2 years of age). 27 (25%) presented with an uropathy (diagnosed by renal US and/or retrograde cystography), boys were overrepresented (46% of boys presented with a uropathy compared to only 14% of girls). 20% of children had a history of UTI, and 44% in the group of children presenting with an uropathy. One hundred and five children (95%) presented with pyelonephritis (and 5 cases of cystitis). 3.2. Exposure to antibiotics Sixty-two children (56%) had been exposed to antibiotics in the year before their UTI episode. 31% had been given several courses in the previous year; the most was 5 courses for 1 child. The data was missing for 3 children (healthcare record not checked and uncertain history with the parents), 3% of the study population. ␤-lactams were the main antibiotic class to which children had been exposed (89% of children) with a slight predominance of cephalosporins. The consumption of others classes was significantly lower: cotrimoxazole for 16% of children, aminoglycosides for 14%, macrolides for 7%, and furanes for 6%. No child had been reported as exposed to other agents in the previous year and particularly to fluoroquinolones (Table 1). The most frequent reasons for prescribing antibiotic were upper respiratory tract infections (otitis, sore throat, rhinopharyngitis, laryngitis) and lower respiratory tract infections (bronchitis, pneumonia, cough) for respectively 52% and 16% of exposed children. The following reasons were UTIs (cystitis or pyelonephritis), prior to the current episode, for 19%. There was no justification for 17% of prescriptions. Most of these antibiotics were given as empirical treatment, without any bacteriological documentation. Forty (64%) of the 62 children had been exposed to antibiotics in the 3 months before the infection, and 58 (93%) in the 6 months before infection. Only 4 children (6%) had not received any antibiotic in the 6 months before infection but between 6 and 12 months; among these, 3 (75%) presented with resistance to 1 or several antibiotic classes. 3.3. Results of cultures E. coli was the most frequent bacterium (78%), followed by Proteus spp. (9% including 7 P. mirabilis and 1 P. vulgaris), and Enterococcus spp. (4%). The others identified pathogens were: others enterobacteria (Enterobacter cloacae 3%, Klebsiella oxytoca 2%), and coagulase negative staphylococcus (1%). Pseudomonas aeruginosa was identified in 2 UMC from hospitalized children, one of who presented with a severe uropathy. 3.4. Antibiotic resistance and uropathy Ninety-three percent of the 27 children presenting with uropathy had been exposed to antibiotics in the previous year and 81% presented resistance to 1 or several antibiotics classes. The presence of an uropathy was not significantly correlated to an

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Table 2 Susceptibility profiles of Escherichia coli urinary strains (%). Résultats des antibiogrammes des isolats urinaires d’Escherichia coli (%).

analysis, after adjusting, proved the correlation between the antibiotic treatment and antibiotic resistance to the agent used, and a significant relationship after exposure to parenteral 3rd GC (p = 0.008) or cotrimoxazole (p = 0.0027). Antibiotic treatment, whatever the agent, in the previous 12 months was correlated to an increased resistance in most classes, the difference reaching the threshold of significance for amoxicillin (p = 0.02) and 1st GC (p = 0.03).

Sensitivity of strains

Amoxicillin Amox-clav Cephalotin Cefixim Cefotaxime Imipenem Cotrimoxazole Nalidixic acid Ciprofloxacin Gentamycin Nitrofurantoine Fosfomycin

Susceptible (%)

Intermediate (%)

Resistant (%)

40 65 43 94 95 100 74 91 93 99 100 100

2 19 44 1 0 0 1 0 0 0 0 0

58 16 13 5 5 0 25 9 7 1 0 0

3.5.2. Analysis after Bonferroni correction No difference significant was found concerning exposure to antibiotics all agents included after using Bonferroni correction (Table 4). Nevertheless the agent-by-agent analysis confirmed a significant difference in resistance after exposure to cotrimoxazole (p = 0.0027). 4. Discussion

over-risk of resistance according to the univariate analysis, even if there was a trend (p = 0.15).

The 4 main lessons drawn from this prospective study of UTIs in pediatrics were:

3.5. Antibiotic resistance in E. coli and correlation with exposure to antibiotics

• the severity of clinical presentations; • a level of antibiotic resistance comparable that of complicated UTIs in adults; • a globale correlation between exposure to antibiotics in the previous 12 months and antibiotic resistance of isolated bacteria; • the frequency of resistance to fluoroquinolones in a population not exposed to these agents.

3.5.1. Univariate analysis The susceptibility profile of E. coli strains is presented in Table 2. The rate of resistance to amoxicillin was unusually high (60%) with a partial restoration of susceptibility by clavulanic acid (35% of strains intermediate or resistant to the combination). Almost 25% of the strains were resistant to cotrimoxazole. Four children (3 girls and 1 boy) carried a strain of E. coli resistant to oral and injectable 3rd GC, in 2 cases because of broad-spectrum ␤-lactamase (BLSE), in 2 others cases because of hyperproduction of cephalosporinase; 2 of these 4 children presented with an uropathy. The antibiotic resistance data of E. coli strains according to the previous exposure to antibiotics (Table 3) demonstrates a globally increased risk in children exposed to 1 or several antibiotics in the year before the infection. The agent-by-agent

The reported series of adult UTIs managed in healthcare institutions often present high rates of cystitis complicated or not [8]; our population presented almost exclusively with pyelonephritis, 25% of which were associated to an underlying uropathy, infections the specific severity of which is well documented in children [9]. This stresses the importance of having effective available antibiotics in these cases.

Table 3 Escherichia coli susceptibility (%) according to antibiotic exposure in the previous 12 months, after adjustement for age, sex, and uropathy. Sensibilité (%) chez Escherichia coli selon l’exposition antibiotique dans les 12 mois précédant, après ajustement sur l’âge, le sexe et la présence d’une uropathie. Antibiotic treatment

Amoxicillin Amox-clav Cephalotin Cefixim Cefotaxime Imipenem Cotrimoxazole Gentamycin Acnalidixic Ciprofloxacin Nitrofurantoine Fosfomycin

Exposure to the agent

Exposure to any antibiotic

Yes (%)

No (%)

p

Yes (%)

No (%)

p

33 69 43 89 82 NA 8 100 NA NA 100 NA

41 62 44 93 95 NA 82 96 90 92 100 100

0.49 0.46 0.69 0.06 0.008 NA 0.0027 1 NA NA NA NA

29 64 35 91 93 100 64 98 89 91 100 100

54 64 54 97 97 100 85 100 92 95 100 100

0.02 0.88 0.03 0.36 0.91 NA 0.09 0.94 0.84 0.25 NA NA

NA: not applicable (no documented previous exposure to this agent). Bold elements: significant results.

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Table 4 Escherichia coli susceptibility (%), according to exposure to antibiotics families in the previous 12 monthsa , after a Bonferroni-type test. Sensibilité chez Escherichia coli (%) selon l’exposition aux classes antibiotiques dans les 12 mois précédanta , après analyse de type Bonferroni. Antibiotic treatment

Betalactams Quinolones Aminoglycosides Sulfamides

Exposure to the agent

Exposure to any antibiotic

Yes (%)

No (%)

p

Yes (%)

No (%)

p

31 NA 100 8

48 NA 99 85

0.11 NA 0.97 0.0027

29 64 98 89

51 85 100 92

0.03 0.84 0.94 0.09

NA: not applicable (no documented previous exposure to any antimicrobial agent). a After adjustment for age, sex, and uropathy when present.

The bacterial species and the level of antibiotic resistance in our population was similar to those currently observed in France in adults [5,6,10,11]. The resistance of E. coli to amoxicillin and cotrimoxazole, concerning respectively more than 50% and 25% of strains, confirmed the impossibility to use these agents for the empirical treatment of pediatric UTIs. The resistance to 3rd GC reached 5%, a worrying rate compared to the 0% reported by Vu Thien in the study of a French pediatric population in 1998 (p < 0.001) [12]. Four children in our series were infected by an enterobacterium resistant to 3rd GC; 3 had been exposed antibiotics in the previous 12 months, and the 4th child, even if not exposed directly, was an 11-day-old neonate the mother of which had received 3rd GC for a UTI during her pregnancy. Many authors had already reported the correlation between exposure to antibiotics and the risk of bacterial resistance, both at the individual and community level [13]. Our results are similar and stress the contribution of the healthcare records for data collection, whereas taking history from patients is rarely reliable (forgetting treatments, confusion between antibiotics and other therapeutic classes, etc.). The healthcare records allow documenting not only exposure but also the reasons for antibiotic use; our results stress the very high percentage of prescriptions for upper or lower respiratory tract infection, the epidemiology of which is known to be more often viral. This means that efforts for the non-prescription of antibiotics should be first made in these cases [3,14]. The effect of previous antibiotic prescriptions on the ecology of UTIs has already been reported in several studies conducted in children [15–17] as well as in adults [10,18–20], but with study periods limited to 3 or 6 months before the studied episodes. For example, Paschke et al. reported, in their series of pediatric UTIs, a correlation between amoxicillin and resistance to this agent after exposure in the 60 days before the episode; no significant association was identified beyond this time range [21]. Two other authors identified a risk of resistance related to antibiotic treatment in the 6 months before a UTI, with for 1 author [22] a 23-fold increased risk for antibiotic resistance after prolonged antibiotic therapy (> 4 weeks), and for the other [23] a 20% increase of strains resistant to cefotaxim in children presenting with a uropathy and having received a prolonged antibiotic prophylaxis (97% of susceptible strains in children without antibioprophylaxis versus 73% in the others). But, these 2 authors had specifically studied children with particular terrains justifying a prolonged antibiotic therapy. We, on

the contrary, chose to study to a global pediatric population, as is usually encountered in routine French hospital practice and extended to 12 months the period during which previous antibiotic therapy, whatever the reason for its use, was correlated to an increased risk of resistance in strains responsible for the UTI. The finer study of delay between exposure to antibiotics and antibiotic resistance in our study shows that limiting the analysis of previous antibiotic therapy to 6 months before the infection would allow identifying most of the children at risk of resistance (93%). Nevertheless, our results also prove the potential impact of antibiotic therapy received more than 6 months before the infection, since 3 of the 4 children not exposed to antibiotics in the 6 months before the UTI but only in the previous 6 to 12 months, were infected by strains resistant to 1 or several antibiotic classes. The method used in most older studies on this issue limited the study period to 3 or 6 months, not allowing any investigation beyond that period. The authors of a few more recent studies extended the investigation period to 12 months and presented conclusions similar to ours. Thus, Arslan et al., in a 2005 study, reported a significant increase of resistance of E. coli urinary isolates to ciprofloxacin in patients having been exposed to fluoroquinolones in the previous 12 months (p < 0.001) [24]. Likewise, the authors of a recent study focusing exclusively on adult UTIs (uncomplicated cystitis) identified a correlation between exposure to trimethoprim or ciprofloxacin in the previous year, and E. coli antibiotic resistance, with an increase of the risk correlated to the number of antibiotic courses [25]. The limited number of children exposed to antibiotics more than 6 months before the UTI in our series, requires confirming these results by a larger study, before considering any modification of the current recommendations. The limitations of our study are related to the small population sample, accounting for the loss of statistical significance after the Bonferonni correction. Nevertheless, this limitation does not prevent taking into account the results: a trend to more resistance in isolates from children exposed to antibiotics in the year before the UTI (or whose mother had been exposed for neonates). The E. coli antibiotic resistance data in our series was compared to that of 2 other studies conducted at the same period (2009–2011) and in the same region (Haute-Normandie), but for adult UTIs. The rate of resistance to 3rd GC and fluoroquinolones observed in pediatrics (respectively 5% and 7%) was significantly superior to those reported for a series of uncomplicated non-recurrent cystitis in female patients 18 to 65 years

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of age (respectively 0.7% and 3.5%) [5], and close to those of a cohort of female patients 18 to 65 years of age, studied in routine practice by UMC in a community laboratory (population with various presentations, recurrent or complicated UTIs, including healthcare related ones; with rates of resistance of respectively 2% and 8%) [6]. The comparison of these 3 series suggests the major impact of previous exposure to antibiotics, know to be less important in young adults without any co-morbidity (in this case female patients presenting with uncomplicated cystitis) compared to children and adults presenting with co-morbidities [3]. Nevertheless, previous exposure to antibiotics does not explain everything as demonstrated by the 7% of E. coli resistant to fluoroquinolones, in children never exposed to this treatment. These results prove the impact of the pressure of selection of antibiotics on the collective level, as well as a probable proportion of inter-human and/or environmental contamination. They stress the importance of large scale antibiotic stewardship at every level and especially in veterinarian medicine, the National Agency of Veterinarian Drugs having reported a 12% increase in the level of exposure to antibiotics in animals, between 1999 and 2010 [26]. 5. Conclusion The results of the study of UTIs in a pediatric unit, revealed the worryingly high rate of bacterial resistance, higher to the one currently observed in adults without any co-morbidity, and correlated to individual exposure to antibiotics in the previous 12 months. Nevertheless, the previous antibiotic treatments do not explain everything, and suggest the implication of environmental, inter-human, or oro-fecal contamination, especially for strains resistant to fluoroquinolones. Disclosure of interest The authors declare that they have no conflicts of interest concerning this article. References [1] Vachvanichsanong P. Urinary tract infection: one lingering effect of chilhood kidney disease – review of the litterature. J Nephrol 2007;20:21–8. [2] Doganis D, Siafas K, Mavrikou M, Issaris G, Martirosova A, Perperidis G, et al. Does early treatment of urinary tract infection prevent renal damage? Pediatrics 2007;120(4):922–8. [3] Sabuncu E, David J, Bernède-Bauduin C, Pépin S, Leroy M, Boëlle PY, et al. Significant reduction of antibiotic use in the community after a nation wide campaign in France, 2002–2007. PLos Med 2009;6(6):e1000084. [4] Dommergues J-P. Carnet de santé de l’enfant : pratique quotidienne. In: EMC – Pédiatrie – Maladies infectieuses. Paris: Elsevier Masson; 2010. p. 1–7 [Article 4-002-F-55]. [5] Etienne M, Frebourg N, Lefebvre E, Pons J, Caron F.Uncomplicated and non recurrent acute cystitis: much less antibiotic resistance than in other series of community-acquired urinary tract infections. 2010.

[6] Fabre R, Mérens A, Lefebvre F, Epifanoff G, Cerutti F, Pupin H, et al. Susceptibility to antibiotics of Escherichia coli isolated from communityacquired urinary tract infections. Med Mal Infect 2010;40(10):555–9. [7] Afsssaps. www.infectiologie.com/site/medias/ documents/consensus/ afssaps-inf-urinaires-enfant-reco.pdf [8] Elkharrat D, Arrouy L, Benhamou F, Dray A, Grenet J, Le Corre A. Épidemiologie de l’infection urinaire communautaire de l’adulte en France. In: Lobel B, Soussy CJ, editors. Les infections urinaires. Springer; 2007. p. 1–20. [9] Jakobsson B, Jacobson SH, Hjalmås K. Vesico-ureteric reflux and other risk factors for renal damage: identification of high- and low-risk children. Acta Paediatr 1999;Suppl. 88(431):31–9. [10] Conseil scientifique de l’ONERBA. www.onerba.org/IMG/pdf/onerba rapport2008 LD.pdf [11] Pangon B, Chaplain C. Pyélonéphrite aiguë : bactériologie et évolution des résistances. Pathol Biol 2003;51:503–7. [12] Vu Thien H. Sensibilité aux antibiotiques des bactéries isolées dans les infections urinaires en pédiatrie. Arch Pediatr 1998;5(Suppl. 3):226–8. [13] Sharland M, SACAR Paediatric Subgroup. The use of antibacterials in children: a report of the Specialist Advisory Committee on Antimicrobial Resistance (SACAR) Paediatric Subgroup. J Antimicrob Chemother 2007;60(Suppl. 1):15–26. [14] Afssaps. www.infectiologie.com. Infections-respir-hautesrecommandations.pdf [15] Cantón R, Novais A, Valverde A, Machado E, Peixe L, Baquero F, et al. Prevalence and spread of extended-spectrum-␤-lactamase-producing Enterobacteriaceae in Europe. Clin Microbiol Infect 2008;14:144–53. [16] Pitout JD, Nordmann P, Laupland KB, Poirel L. Emergence of Enterobacteriaceae producing extended-spectrum-␤-lactamases (ESBLs) in the community. J Antimicrob Chemother 2005;56:52–9. [17] Fritzsche M, Ammann RA, Droz S, Bianchetti MG, Aebi C. Changes in antimicrobial resistance of Escherichia coli causing urinary tract infections in hospitalized children. Eur J Clin Microbiol Infect Dis 2005;24: 233–5. [18] Goldstein FW. Antibiotic susceptibility of bacterial strains isolated from patients with community-acquired urinary tract infection in France. Multicentre Study group. Eur J Clin Microbiol Infect Dis 2000;19:112–7. [19] Metlay JP, Strom BL, Asch DA. Prior antimicrobial drug exposure: a risk factor for trimethoprim-sulfamethoxazole-resistant urinary tract infections. J Antimicrob Chemother 2003;51(4):963–70. [20] Hillier S, Roberts Z, Dunstan F, Butler C, Howard A, Palmer S. Prior antibiotics and risk of antibiotic-resistant community-acquired urinary tract infection: a case-control study. J Antimicrob Chemother 2007;60(1): 92–9. [21] Paschke AA, Zaoutis T, Conway PH, Xie D, Keren R. Previous antimicrobial exposure is associated with drug-resistant urinary tract infections in children. Pediatrics 2010;125(4):664–72. [22] Allen UD, MacDonald N, Fuite L, Chan F, Stephens D. Risk factors for resistance to “first-line” antimicrobials among urinary tract isolates of Escherichia coli in children. CMAJ 1999;160(10):1436–40. [23] Lutter SA, Currie ML, Mitz LB, Greenbaum LA. Antibiotic resistance patterns in children hospitalized for urinary tract infections. Arch Pediatr Adolesc Med 2005;159:924–8. [24] Arslan H, Azap OK, Ergönül O, Timurkaynak F, Urinary Tract Infection Study Group. Risk factors for ciprofloxacin resistance among Escherichia coli strains isolated from community-acquired urinary tract infections in Turkey. J Antimicrob Chemother 2005;56(5):914–8. [25] Vellinga A, Tansey S, Hanahoe B, Bennett K, Murphy AW, Cormican M. Trimethoprim and ciprofloxacin resistance and prescribing in urinary tract infection associated with Escherichia coli: a multilevel model. J Antimicrob Chemother 2012;67:2523–30. [26] Chevance A, Moulin G, Chauvin C, Gay E. La consommation des antibiotiques à usage vétérinaire en Fr.

Urinary tract infections in hospital pediatrics: many previous antibiotherapy and antibiotics resistance, including fluoroquinolones.

We studied antibiotic resistance in pediatric UTIs and we evaluated the impact of antibiotic exposure in the previous 12 months, very little French da...
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