|Year : 2020 | Volume
| Issue : 2 | Page : 136-142
High carriage rates of extended-spectrum beta-lactamase-producing enterobacteriaceae in children at admission into paediatric wards of a university teaching hospital in Lagos, Nigeria
Oluwaseun Olaide Jewoola1, Ibidunni Oreoluwa Bode-Sojobi1, Folasade T Ogunsola1, Patrick E Okonji2
1 Department of Medical Microbiology, College of Medicine, University of Lagos, Idi-Araba, Akoka, Lagos, Nigeria
2 Research and Innovation Unit, University of Lagos, Akoka, Lagos, Nigeria
|Date of Submission||09-Jan-2020|
|Date of Decision||19-Feb-2020|
|Date of Acceptance||24-Feb-2020|
|Date of Web Publication||11-Apr-2020|
Prof. Folasade T Ogunsola
Department of Medical Microbiology, University of Lagos, Akoka, Lagos
Source of Support: None, Conflict of Interest: None
Context: Bowel carriage has been identified as the main reservoir of extended-spectrum beta-lactamase-producing Enterobacteriaceae (ESBL-PE) and hospital-acquired infections. There are gaps in the knowledge of trends of these rates, which need to be filled for the development and implementation of hospital surveillance systems and antibiotic stewardship programmes in Nigeria. Aim: This study investigated the carriage rates of ESBL-PE among 273 children admitted to the paediatric wards of a university teaching hospital, Nigeria, using a prospective cohort study design over a 6-month period. Settings and Design: The study explored the role of new and transferred patients in introducing resistant strains of ESBLs into paediatric wards and how quickly paediatric patients that were previously free of resistant strains acquired these within the hospital environment. Materials and Methods: E-swabs (Copan Diagnostics, Italy) were used to obtain rectal samples from participants. Positive colonies were Gram stained and subcultured onto purity plates for further identification, and antibiotic susceptibility pattern of identified ESBL-PE was obtained using a range of antibiotics. Statistical Analysis Used: Data were analysed using SPSS statistics 20 (IBM SPSS Statistics, version 20). Statistical significance was determined using the Chi-square test and Fisher's exact test. A logistic regression analysis was also conducted to identify independent risk factors for colonisation. Results: The findings showed that transferred patients contributed to the introduction of ESBLs into the hospital. Independent multivariate risk factors for colonisation of ESBL-PE were age >10–14 years, instrumentation (odds ratio [OR]: 0.2 [P < 0.05]) and sharing of thermometers (OR: 0.11 [P < 0.05]). Conclusions: The carriage rate of ESBL-PE is high (25.3%) among children, and none-carriers may become colonised within 14 days of hospitalisation.
Keywords: Children, Enterobacteriaceae, extended-spectrum beta-lactamase carriage, extended-spectrum beta-lactamase colonisation, paediatric wards
|How to cite this article:|
Jewoola OO, Bode-Sojobi IO, Ogunsola FT, Okonji PE. High carriage rates of extended-spectrum beta-lactamase-producing enterobacteriaceae in children at admission into paediatric wards of a university teaching hospital in Lagos, Nigeria. Niger Postgrad Med J 2020;27:136-42
|How to cite this URL:|
Jewoola OO, Bode-Sojobi IO, Ogunsola FT, Okonji PE. High carriage rates of extended-spectrum beta-lactamase-producing enterobacteriaceae in children at admission into paediatric wards of a university teaching hospital in Lagos, Nigeria. Niger Postgrad Med J [serial online] 2020 [cited 2020 Nov 28];27:136-42. Available from: https://www.npmj.org/text.asp?2020/27/2/136/282320
| Introduction|| |
Enterobacteriaceae species are normal inhabitants of the gut and environment, and have been reported as a cause of hospital-acquired infections (HAIs). HAIs can be transmitted within the environment of care and are associated with long hospital stay. Patients colonised by resistant bacteria may shed them into their surroundings and transmit to other patients in proximity. Some studies have shown that colonisation by bacteria usually precedes most HAIs. Patients are often colonised with resistant organisms such as methicillin-resistant Staphylococcus aureus, vancomycin-resistant Enterococci and extended-spectrum beta-lactamase-producing Enterobacteriaceae (ESBL-PE), which tends to reflect their high prevalence in clinical samples, and, consequently, are responsible for most outbreaks of infections in hospitals globally.,
Bowel carriage has been identified as the main reservoir of ESBL-PE and HAIs. The resistant organism is frequently associated with poor implementation of infection prevention and control measures., Optimal infection control measures such as hand hygiene, contact precautions and environmental cleaning are the mainstay of preventing infection by these organisms.
In sub-Saharan Africa, there is paucity of data evaluating the rates of carriage and spread of ESBLs PE in hospital units. Studies available in literature have shown prevalence rates with little information on how resistant organisms are spread during hospital admissions, its reservoirs and associated risk factors., These studies focused on the genotypic characteristics of isolates, with few details on their clinical data and external sources of ESBL-introducing organisms into the hospital. In many low- and middle-income countries, the absence of standard treatment guidelines often encourages overprescription of antibiotics by health workers as well as antibiotic overusage, all of which substantially counter efforts to control the spread of known and novel strains of antibiotic-resistant pathogens., Access to antibiotics is easy in Nigeria, and there has been an increasing trend in antibiotic resistance both in the community and the hospital., Two studies from Nigeria have reported high prevalence rates of ESBLs derived from clinical isolates., These studies gave little information on the role of the community isolates on reported prevalence from the hospitals. In Madagascar and Niger, studies were conducted to determine the rates of carriage and acquisition of ESBL-PE among hospitalised paediatric population and malnourished children, respectively., Both studies recorded high carriage rates of 22% and 31% and acquisition rates of 57.1% and 94%, respectively. The knowledge of trends of these rates is necessary for the development and implementation of hospital surveillance systems and antibiotic stewardship programmes in Nigeria.
This study investigated the role of new and transferred patients in introducing resistant strains of ESBLs into paediatric wards. It also evaluated how quickly paediatric patients that were previously free of resistant strains acquired these within the hospital environment.
| Materials and Methods|| |
Ethical approval for this study was sought and granted by the Health Research and Ethics Committee of the Lagos University Teaching Hospital (LUTH), Idi-Araba, Lagos, with protocol number XVI/APP/682 approved by the ethics committee on 18 December 2012.
This was a prospective cohort study conducted on newly admitted inpatients at the paediatric unit of a university teaching hospital (UTH) and lasted for a 6-month period (21 April to 25 October 2014). All children between the ages of 0 and 14 years admitted through the children emergency room, children outpatient clinics (outpatient department) and neonatal ward (NNU) were included in the study. Patients who had been admitted for > 24 h prior to the commencement of the study as well as children whose parents/guardian refused consent were excluded from the study. A total of 273 patients were recruited into the study. The sample size was calculated using Cochran's sample size formula, with an estimated ESBL prevalence rate of 21% as determined in a previous study on ESBL carriage rate among children in a Madagascan hospital. Using this prevalence rate in calculating the sample size:
where Z = critical value at 95% confidence level set at 1.96, d = is the precision at 5% and P is the proportion of the population that have positive yield from blood culture (set at 21%). Hence, the sample size = 1.96 × 1.96 × 0.21 × 0.8/0.05 × 0.05 = 258. A total of 273 patients were, thus, recruited for the study.
Patients were screened for carriage of ESBL-PE on day 1 of entry into the hospital. The rate of acquisition was subsequently determined on days 3, 8 and 14 of admission on patients who had been previously ESBL negative. ESBL-PE were identified among bowel isolates obtained from patients. Two randomly sampled doctors and two nurses who managed patients admitted into paediatric wards were screened weekly for ESBLs. Randomisation of healthcare workers was done by selecting every first doctor or nurse encountered at the patient's bedside and every last doctor or nurse encountered after collection of patients' samples from another ward. Healthcare workers were sampled from two shifts (morning and night), within wards of admission (viz., emergency room, neonatal unit, NNU-D1, children's ward-D2 and children's ward-D3). Cultures were obtained from the environment to detect contamination with ESBL-PE. Environmental samples were taken at different sites within the hospital premises, including sinks, door knobs, washing baths, tap knobs, incubators and buretrols.
Questionnaires were designed to obtain patient demographic data and clinical data (ward of admission, referral centre, comorbidities, exposure to antimicrobial drugs 3 months prior to study, hospitalisation within the previous 12 months, presence of indwelling urinary or vascular catheters or nasogastric feeding), and were administered in person by the investigator. Other relevant information gathered from clinicians included sharing of thermometers, route of drug administration, number and types of antibiotics used in current admission; history of antibiotic use in the last 3 months; history of admission in the past 12 months and type of referral centre. Sixty medical staff members were selected for screening. They included 19 house officers, 9 resident doctors and 32 nurses. Only 48 consented to be a part of the study.
Rectal swabs were used for ESBL screening as research suggests that healthcare-associated ESBL-PE infections are usually preceded by colonisation of the gastrointestinal tract., E-swabs (Copan Italia SpA, Brescia, Italy) were used to obtain rectal samples from the participants. The specimens were kept in re-sealable polyethylene bags and transferred to the department of medical microbiology and parasitology laboratory for processing as quickly as it was possible. Positive colonies were Gram stained and subcultured onto purity plates for further identification. Quality control strains Escherichia coli ATCC 25922 and Klebsiella pneumoniae ATCC 70063 were included in each run as negative and positive controls, respectively. All non-repetitive isolates were identified using the Microbact™ 12A (Oxoid™, Basingstoke, UK) identification kits. The susceptibility pattern of identified ESBL-PE was derived using the following antibiotics: amikacin 30 μg, ceftazidime 30 μg, cefotaxime 30 μg, ciprofloxacin 5 μg, gentamicin 10 μg, aztreonam 30 μg, cefepime 30 μg, cefoxitin 30 μg, meropenem 10 μg and piperacillin-tazobactam 100/10 μg. An interpretative correlate (susceptible, intermediate or resistant) was provided by reference to Clinical and Laboratory Standards Institute (CLSI) guidelines. Previously identified ESBL-PE were confirmed using the 2012 CLSI guidelines ESBL confirmatory test for phenotypic detection of ESBL in Enterobacteriaceae.
Data were analysed using IBM. SPSS statistics for Windows. Version 20.0. Armonk, NY: IBM; 2011 Statistical significance was determined using the Chi-square test and Fisher's exact test. A logistic regression analysis was also used to identify independent risk factors for colonisation and remove confounders. A univariate analysis of potential risk factors for ESBL carriage was done to identify statistically significant relationship between potential risk factors and the probability of carrying an ESBL-PE. Further analysis included a logistic regression analysis to negate confounders that may give false interpretation to the results. An association between a risk factor and ESBL carriage is said to exist if the P value for that risk factor is < 0.05.
| Results|| |
A total of 273 newly admitted patients were recruited into the study over a 6-month period between April and October, 2014. Of these, 166 were males and 107 were females, with a male-to-female sex ratio of 1.6:1.0. [Table 1] shows the demographic profile of the study participants. Thirty-one patients (11.4%) had an illness, whereas 81 patients (29.7%) had been hospitalised within the previous 30 days and another 47 (17.2%) had been hospitalised in the preceding 12 months. Sharing of thermometers was reported in 234 out of the 273 patients (85.7%) and 198 (72.5%) patients had some instrumentation while at the hospital. A total of 28 out of 129 self-referred patients (21.7%) had been administered an antibiotic 3 months prior to hospitalisation, while 24% of ESBL-positive self-referred patients had also been administered an antibiotic 3 months before hospitalization [Table 2]. The rectal carriage rate of ESBL-PE in the admitted children was 25.3% derived from 69 out of the 273 patients who screened positive at entry into the hospital [Figure 1]. The most common strains isolated were K. pneumoniae (44.2%), E. coli (34.2%) and Enterobacter spp. (12.8%). Other Enterobacteriaceae such as Klebsiella oxytoca, Citrobacter freundii and Serratia rubidaea constituted the remaining isolates [Figure 2].
|Table 1: Demographics and clinical characteristics of the respondents (n=273) |
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|Figure 1: Patient distribution according to extended-spectrum beta-lactamase carriage and acquisition rates|
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|Figure 2: Trends of acquired extended-spectrum beta-lactamase-producing Enterobacteriaceae during hospitalisation|
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In vitro sensitivity of the 143 isolates to the tested antibiotics revealed different patterns of susceptibility or resistance to the tested antibiotics. Overall, ESBL-producing isolates exhibited high resistance to cefotaxime (98.6%), ceftazidime (95.1%), aztreonam (86.0%), gentamicin (74.8%), ciprofloxacin (72.7) and cefepime (58.7) [Table 3]. Meropenem demonstrated good activity in 108 (75.5%) of the 143 isolates, followed by cefoxitin with 50 sensitive isolates (34.97%). There was intermediate susceptibility to piperacillin-tazobactam in 71 isolates (49.6%), amikacin in 67 isolates (46.8%), cefepime in 46 isolates (32.2%) and ciprofloxacin in 39 isolates (27.3%). Fewer isolates of Enterobacter spp. and Klebsiella spp. were susceptible to amikacin at 0.05% and 18.9%, respectively, compared than E. coli isolates at 38.8%. No ESBL-PE was detected from the hands of healthcare workers tested. Only 7 (6.25%) of the 112 environmental samples tested for ESBL were positive.
|Table 3: Antibiogram and antibiotic profile of common extended spectrum beta lactamase-producing Enterobacteriaceae phenotypes isolated from patients |
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Factors in the study which suggested an association with ESBL carriage were instrumentation (P = 0.007), number of days of hospital admission prior to referral (P = 0.02), sharing of thermometers (P < 0.000), route of drug administration (P = 0.02), number of antibiotics used in current admission (P = 0.01) and age group (P < 0.00). Potential risk factors which showed no evidence of association with ESBL carriage were history of antibiotic use in the last 3 months, history of admission in the past 12 months and type of referral centre.
Age group, instrumentation and shared thermometers came out as independent risk factors for acquiring ESBLs on the ward. The most significant group with potential risk for ESBL carriage were early adolescents aged >10–14 years with an odds ratio (OR) of 8.3 (P < 0.05) of acquiring ESBL. All patients in this age group were eight times more likely to be colonised with ESBL than children in other age groups. Instrumentation was identified as a risk factor as children who had no instrumentation were five times less likely to become colonised with ESBL than those who had some form of instrumentation while on admission (OR: 0.2 [P < 0.05]). Sharing of thermometers was a risk factor, and patients who shared thermometers were approximately nine times more likely to get colonised or acquire ESBL than those who did not (OR: 0.11 [P < 0.05]) [Table 4]. Multivariate regression analysis showed that the risk factors for ESBL acquisition during hospitalisation such as age group (P = 0.014), sex (P = 0.008), ward of admission (P = 0.02), number of antibiotics used during hospitalisation (P < 0.000), route of drug administration (P = 0.02) and sharing of thermometers (P < 0.000) that were significant by univariate analysis were not statistically significant by multiple regression analysis and therefore are not independent risk factors.
|Table 4: Independent multivariate risk factors for rectal carriage of extended-spectrum beta-lactamase at hospital admission at Lagos University Teaching Hospital |
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| Discussion|| |
This 6-month prospective cross-sectional study determined the carriage and hospital acquisition rates of ESBL in the gut of newly admitted children at our hospital. It also identified environmental reservoirs as well as risk factors that promote the spread of resistant organisms in the hospital environment. There was a carriage rate of 25.3% (69 of 273 patients), in all patients screened at entry. This implies that one out of every five patients admitted into the paediatric unit was colonised with ESBL. This suggests that the isolates were either acquired from the referral centres or from the community.
The overall acquisition rate was estimated at 22.1% over 14 days, while the highest acquisition rate was within the first 3 days of admission. This suggests a relatively high transmission rate of microorganisms within the hospital and also suggests poor infection control procedures. Similar rates have been reported from other African countries where the rectal carriage rate was 21.2%, 31.3% and 32.6% in Madagascar, Niger and Guinea-Bissau, respectively.,, In addition, most of the patients in these studies acquired resistant strains within 3–8 days of admission as observed in our study. This study adds novel insight to the carriage rates of ESBL among children in Nigeria as there is currently no published data showing carriage rates of ESBL in children in Nigeria with which to compare our data.
In determining the rate of carriage, Andriatahina et al. re-screened all previously colonised and non-colonised patients at hospital entry and at discharge or after 30 days to arrive at an acquisition rate of 57.1%. This study, on the other hand, focused on determining the time it took to acquire ESBL-resistant organisms while on admission within a 14-day follow-up period. The overall acquisition rate of 22.1% was lower. A possible explanation for the lower rate is that re-screening all previously colonised and non-colonised at discharge was not conducted as it was not the focus of this study. Such analysis will likely result in higher values of acquisition rate. Consequently, it becomes unreasonable to compare acquisition rate in the study cohort with the findings from the study by Andiatahian et al.
Antibiotic use positively correlated with ESBL carriage at admission. Among all the children that were colonised on admission, about one-third (29%) had been on antibiotics, while more than half (58%) had been referred from other healthcare facilities. In this study, two children referred from traditional birth attendants were infected with ESBL, while one of them, in addition, had a history of antibiotic use, suggesting that the use of antibiotics occurred in these traditional medicine settings and may account for some of the antibiotic selection pressure-driving resistance in the community.
Findings from this study show that transferred patients contributed to the introduction of ESBLs into our UTH because 69 out of the 273 patients (25%) were positive at entry. Of these, 29 patients (42%) were self-referred and 13 (48%) had used an antibiotic in the 3 months preceding the admission to the hospital. The findings also confirm the role of antibiotic selection pressure in the emergence of resistant microorganisms and further confirm the findings from the study by Levy in 1976 which showed that antibiotic selective pressure is responsible for the emergence of resistant organisms. In addition, this study also shows how resistant organisms could easily arise and spread among shared patients. About half of the patients (50.7%) who were ESBL carriers at entry had been previously admitted for an infection which included pneumonia, meningitis and gastroenteritis. These infections would have required treatment with antibiotics and inpatient admission, suggesting that they might have acquired resistant organisms from a healthcare facility.
Swabs from the hands of 48 healthcare workers yielded no ESBL-PE. The availability of alcohol-based hand rubs and compliance with the practice of hand hygiene among the healthcare workers that were screened could, perhaps, account for the observed absence of organisms in the study. ESBL-producing E. coli and K. pneumoniae were, however, isolated from sinks, buretrols, door knobs, washing baths, taps and basin. The finding of these organisms on doorknobs and taps further suggests hand carriage of these organisms despite the inability to grow them from the hands of healthcare workers. In this study, the independent multivariate risk factors for colonisation of ESBL-PE were age >10–14 years, instrumentation and sharing of thermometers compared with non-colonisers throughout the study. This study showed that children aged >10–14 years were eight times more likely to be colonised with ESBL than neonates, infants and pre-school and school-aged children admitted in the LUTH. There were six children in this group, There were six children in this category, and 25% of them had a history of antibiotic use in the past 3 months and were five times more likely to have had Instrumentation. In addition, 15% of them had a history of hospital admission in the last 12 months. These preceding potential risk factors and small sample size may explain the peculiarity in this group. These children are also likely to be more ambulant in the wards, predisposing them to more chances of acquiring organisms in the hospital environment or from peers. Sharing of thermometers was also identified as an independent risk factor in this study. Thermometers were not shared if used via the rectum. The study shows that patients who did share were approximately nine times more likely to be colonised with ESBL-PE than those who did not [Table 4].
| Conclusion|| |
This study has shown that carriage rate of ESBL-PE is high (25.3%) among children admitted at the LUTH and 22.1% of the children who were none-carriers may become colonised within 14 days of hospitalisation. Findings from these results would have been more specific if molecular typing had been done and if the children were followed up for a longer period. Nevertheless, the study showed that children who shared thermometers and who had instrumentation were five and nine times (respectively) more likely to acquire ESBL on the wards. In addition, children between the ages of 10 and 14 years were more at risk for ESBL acquisition on the ward. The study also showed that at least 25% of ESBLs were imported into the hospital, and over a third of these were from referred patients.
The authors acknowledge provision of rectal swabs and chrom agar by Copan Diagnostics Italia.
Financial support and sponsorship
Conflicts of interest
There are no conflicts of interest.
| References|| |
Zhanel GG, DeCorby M, Adam H, Mulvey MR, McCracken M, Lagacé-Wiens P, et al
. Prevalence of antimicrobial-resistant pathogens in Canadian hospitals: Results of the Canadian Ward Surveillance Study (CANWARD 2008). Antimicrob Agents Chemother 2010;54:4684-93.
Horcajada JP, Shaw E, Padilla B, Pintado V, Calbo E, Benito N, et al
. Healthcare-associated, community-acquired and hospital-acquired bacteraemic urinary tract infections in hospitalized patients: A prospective multicentre cohort study in the era of antimicrobial resistance. Clin Microbiol Infect 2013;19:962-8.
Paterson DL, Singh N, Rihs JD, Squier C, Rihs BL, Muder RR. Control of an outbreak of infection due to extended-spectrum beta-lactamase—producing Escherichia coli
in a liver transplantation unit. Clin Infect Dis 2001;33:126-8.
Donskey CJ. Antibiotic regimens and intestinal colonization with antibiotic-resistant gram-negative bacilli. Clin Infect Dis 2006;43 Suppl 2:S62-9.
Espinosa de los Monteros LE, Silva-Sanchez J, Jiménez LV, Rojas T, Garza-Ramos U, Valverde V. Outbreak of infection by extended-spectrum beta-lactamase SHV-5-producing Serratia marcescens
in a Mexican hospital. J Chemother 2008;20:586-92.
Cotton MF, Wasserman E, Pieper CH, Theron DC, van Tubbergh D, Campbell G, et al
. Invasive disease due to extended spectrum beta-lactamase-producing Klebsiella pneumoniae
in a neonatal unit: The possible role of cockroaches. J Hosp Infect 2000;44:13-7.
Calbo E, Freixas N, Xercavins M, Riera M, Nicolás C, Monistrol O, et al
. Foodborne nosocomial outbreak of SHV1 and CTX-M-15-producing Klebsiella pneumoniae
: Epidemiology and control. Clin Infect Dis 2011;52:743-9.
Zaidi AK, Thaver D, Ali SA, Khan TA. Pathogens associated with sepsis in newborns and young infants in developing countries. Pediatr Infect Dis J 2009;28:S10-8.
Martinez-Aguilar G, Alpuche-Aranda CM, Anaya C, Alcantar-Curiel D, Gayosso C, Daza C, et al
. Outbreak of nosocomial sepsis and pneumonia
in a newborn intensive care unit by multiresistant extended-spectrum beta-lactamase-producing Klebsiella pneumoniae
: High impact on mortality. Infect Control Hosp Epidemiol 2001;22:725-8.
Lonchel CM, Meex C, Gangoué-Piéboji J, Boreux R, Assoumou MC, Melin P, et al
. Proportion of extended-spectrum ß-lactamase-producing Enterobacteriaceae
in community setting in Ngaoundere, Cameroon. BMC Infect Dis 2012;12:53.
Soge OO, Queenan AM, Ojo KK, Adeniyi BA, Roberts MC. CTX-M-15 extended-spectrum (beta)-lactamase from Nigerian Klebsiella pneumoniae
. J Antimicrob Chemother 2006;57:24-30.
Allegranzi B, Bagheri Nejad S, Combescure C, Graafmans W, Attar H, Donaldson L, et al
. Burden of endemic health-care-associated infection in developing countries: Systematic review and meta-analysis. Lancet 2011;377:228-41.
Magwenzi MT, Gudza-Mugabe M, Mujuru HA, Dangarembizi-Bwakura M, Robertson V, Aiken AM. Carriage of antibiotic-resistant Enterobacteriaceae
in hospitalised children in tertiary hospitals in Harare, Zimbabwe. Antimicrob Resist Infect Control 2017;6:10.
Oyetunde OO, Olugbake OA, Famudehin KF. Evaluation of use of antibiotic without prescription among young adults. Afr J Pharm Pharmacol 2010;4:760-2.
Afunwa RA, Odimegwu DC, Iroha RI, Esimone CO. Antimicrobial resistance status and prevalence rates of extended spectrum beta-lactamase (ESBL) producers isolated from a mixed human population. Bosn J Basic Med Sci 2011;11:91-6.
Ogbolu DO, Daini OA, Ogunledun A, Alli AO, Webber MA. High levels of multidrug resistance in clinical isolates of Gram-negative pathogens from Nigeria. Int J Antimicrob Agents 2011;37:62-6.
Raji MA, Jamal W, Ojemhen O, Rotimi VO. Point-surveillance of antibiotic resistance in Enterobacteriaceae
isolates from patients in a Lagos Teaching Hospital, Nigeria. J Infect Public Health 2013;6:431-7.
Andriatahina T, Randrianirina F, Hariniana ER, Talarmin A, Raobijaona H, Buisson Y, et al
. High prevalence of fecal carriage of extended-spectrum ß-lactamase-producing Escherichia coli
and Klebsiella pneumoniae
in a pediatric unit in Madagascar. BMC infect Dis 2010;10:204.
Woerther PL, Angebault C, Jacquier H, Hugede HC, Janssens AC, Sayadi S, et al
. Massive increase, spread, and exchange of extended spectrum β-lactamase-encoding genes among intestinal Enterobacteriaceae
in hospitalized children with severe acute malnutrition in Niger. Clin Infect Dis 2011;53:677-85.
Cochran WG. Sampling Techniques. 3rd
ed. New York: John Wiley and Sons; 1977.
Herindrainy P, Randrianirina F, Ratovoson R, Ratsima Hariniana E, Buisson Y, Genel N, et al
. Rectal carriage of extended-spectrum beta-lactamase-producing gram-negative bacilli in community settings in Madagascar. PLoS One 2011;6:e22738.
Luiten EJ, Hop WC, Endtz HP, Bruining HA. Prognostic importance of gram-negative intestinal colonization preceding pancreatic infection in severe acute pancreatitis. Results of a controlled clinical trial of selective decontamination. Intensive Care Med 1998;24:438-45.
Clinical and Laboratory Standards Institute. Methods for Dilution Antimicrobial Susceptibility Tests for Bacteria that Grow Aerobically; Approved Standard. MO7-A9. 9th
ed. Wayne, PA: Clinical and Laboratory Standards Institute; 2012.
Isendahl J, Turlej-Rogacka A, Manjuba C, Rodrigues A, Giske CG, Nauclér P. Fecal carriage of ESBL-producing E. coli
and K. pneumoniae
in children in Guinea-Bissau: A hospital-based cross-sectional study. PLoS One 2012;7:e51981.
Levy SB, FitzGerald GB, Macone AB. Changes in intestinal flora of farm personnel after introduction of a tetracycline-supplemented feed on a farm. N
Engl J Med 1976;295:583-8.
[Figure 1], [Figure 2]
[Table 1], [Table 2], [Table 3], [Table 4]