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High proportion of multidrug-resistant organisms in children hospitalized abroad
ARTICLE IN PRESS American Journal of Infection Control 000 (2019) 1−3
Contents lists available at ScienceDirect
American Journal of Infection Control journal homepage: www.ajicjournal.org
Brief Report
High proportion of multidrug-resistant organisms in children hospitalized abroad Kazuhiro Uda MD a, Takanori Funaki MD a, Kensuke Shoji MD a, Akira Kato MSc b, Isao Miyairi MD a,* a b
Division of Infectious Diseases, Department of Medical Subspecialties, National Center for Child Health and Development, Setagaya-ku, Tokyo, Japan Clinical Microbiology Laboratory, Department of Clinical Laboratory Medicine, National Center for Child Health and Development, Setagaya-ku, Tokyo, Japan
Key Words: Antibiotic-resistant bacteria Active screening Multidrug-resistant bacteria
Our infection control team initiated active screening for multidrug-resistant organisms (MDROs) among children who had been hospitalized abroad before their admission to our hospital. MDROs were detected in 19 of 34 cases (56%), including 3 isolates of Enterobacteriaceae harboring carbapenemase genes still rare in Japan. Early recognition of MDROs by screening this population may be required to avoid the introduction of new modes of resistance into the hospital environment. © 2019 Association for Professionals in Infection Control and Epidemiology, Inc. Published by Elsevier Inc. All rights reserved.
The emerging spread of multidrug-resistant organisms (MDROs) is a serious global problem.1,2 Medical tourists, expatriates, and travelers represent a source of introducing MDROs that were previously absent in the community.3 The early recognition of MDROs and preemptive infection control is important. However, the targets and tools for screening have not been established, particularly in pediatrics. In December 2014, our infection control team initiated active screening for MDROs in children who had been previously hospitalized abroad before their admission to our hospital. The aim of this study is to evaluate the proportion and characteristics of MDROs identified with active screening for children previously hospitalized abroad.
METHODS
November 2014 and December 2017. Patients’ demographic data, underlying disease, past medical history, country of previous hospitalization, and duration of hospital stay were extracted from electronic medical records. All patients admitted to our institution are required to fill out a checklist prior to hospitalization, which includes questions about history of hospitalization abroad. The preemptive infection control strategy in our institution is shown in Supplementary Figure S1. All statistical analyses were performed using IBM SPSS Statistics version 22 (IBM Corporation, Tokyo, Japan). The Fisher exact test for categorical variables and the Mann−Whitney U test for continuous variables were used for the analyses. A P value <0.05 (2sided) was considered significant. The hospital’s institutional review board approved this study (NCCHD-1793).
Study population
Screening and definition of MDROs
This observational study was conducted at the National Center for Child Health and Development in Tokyo, Japan. Our hospital is a tertiary children’s hospital with 490 beds, including a pediatric intensive care unit, a neonatal intensive care unit, and a pediatric transplant center. We included patients aged <18 years hospitalized between
We performed active surveillance only at the time of patient admission. Stool or rectal swab samples were obtained and underwent screening using blood agar and antibiotic-containing media as follows: Drigalski Agar, Modified (Becton, Dickinson and Company, Tokyo, Japan) and CHROMagar mSuper CARBA/ESBL (Kanto Chemical, Tokyo, Japan). We used an automated identification and susceptibility testing system (BD Phoenix, Becton, Dickinson and Company, Tokyo, Japan or MicroScan Walkaway, Beckman Coulter Inc, Tokyo, Japan). Antimicrobial susceptibility was determined according to the breakpoints set by the Clinical and Laboratory Standard Institute criteria [M100-S21]. Carbapenemase-producing genes were identified with the Cica Geneus Carbapenemase Genotype Detection KIT (Kanto Chemical, Tokyo, Japan). MDROs were defined as follows: AmpC-type b-lactamase (AmpC)−producing organisms,
* Address correspondence to Isao Miyairi, MD, Division of Infectious Diseases, Department of Medical Subspecialties, National Center for Child Health and Development, 2-10-1 Okura, Setagaya-ku, Tokyo 157-8535, Japan. E-mail address: [email protected] (I. Miyairi). Conflicts of interest: None to report. Author contributions: K.U. and T.F. contributed to conceptualizing the study and collected data. K.U. drafted the manuscript and performed the data analyses. K.S. and A.K. contributed to the critical revision of the manuscript. I.M. revised the manuscript and supervised the study as the corresponding author.
https://doi.org/10.1016/j.ajic.2019.08.013 0196-6553/© 2019 Association for Professionals in Infection Control and Epidemiology, Inc. Published by Elsevier Inc. All rights reserved.
ARTICLE IN PRESS K. Uda et al. / American Journal of Infection Control 00 (2019) 1−3
2
carbapenemase-producing Enterobacteriaceae (CPE), extendedspectrum b-lactamase (ESBL)−producing Enterobacteriaceae, and vancomycin-resistant Enterococcus (VRE) spp.
RESULTS Active screening was performed for 34 cases. The median age was 32 months (interquartile range, 15-82 months) and 23 (68%) were male patients. Previous hospitalizations in Asian countries outside of Japan were most common (29 cases, 85%), and were concentrated in Eastern Asia. Twenty-seven cases (79%) had underlying diseases, and visits for their treatment and diagnosis were the most common reason for entering our hospital. There were no patients who were evacuated or transferred directly from a foreign hospital. MDROs were detected in 19 cases (56%), including CPE (3 samples),
Table 1 Demographic data, locations of previous hospitalizations, and the microorganisms in cases with or without MDROs
Age (months)* Sex (male) Nationality Non-Japanese Underlying diseases Neurologic Gastrointestinal Liver Urologic Hematologic/Oncologic Endocrine Genetic None Reason for visit Seeking treatment Seeking diagnosis Sick during travel Immigrant Othery Location of the previous admission Asia Eastern Asia South-Eastern Asia Southern Asia Central Asia Western Asia Europe North America Central/South America Africa Duration (days) of admission in our hospital* Microorganism (including duplications) Escherichia coli (ESBL) Escherichia coli (AmpC) Escherichia coli (ESBL+AmpC) Escherichia coli (NDM) Klebsiella pneumoniae (ESBL) Klebsiella pneumoniae (NDM) Klebsiella pneumoniae (KPC) Citrobacter braakii (AmpC) Enterobacter cloacae (AmpC) Enterococcus faecium (VRE)
MDROs (+) n = 19
MDROs (−) n = 15
P Value
32 (15-82) 13 (68%)
32.5 (16-83) 10 (67%)
> .99 > .99
19 (100%) 16 (84%) 1 (5%) 1 (5%) 3 (16%) 4 (21%) 3 (16%) 4 (21%) 0 (0%) 3 (16%)
14 (93%) 11 (73%) 3 (20%) 0 (0%) 4 (24%) 0 (0%) 2 (13%) 1 (7%) 1 (7%) 4 (27%)
.44 .67 > .99 > .99 .67 .11 1.00 .35 .44 .67
6 (32%) 10 (53%) 0 (0%) 3 (16%) 0 (0%)
6 (40%) 6 (40%) 1 (7%) 1 (7%) 1 (7%)
.72 .51 .44 .61 .44
17 (89%) 11 (58%) 3 (16%) 3 (16%) 0 (0%) 0 (0%) 0 (0%) 0 (0%) 1 (5%) 1 (5%) 11 (6-30)
12 (80%) 3 (20%) 5 (33%) 2 (13%) 1 (7%) 1 (7%) 1 (7%) 2 (13%) 0 (0%) 0 (0%) 11 (8-32)
14 1 1 1 1 1 1 1 1 1
.63 — — — — — .44 .18 > .99 > .99 > .99
N/A N/A N/A N/A N/A N/A N/A N/A N/A N/A
AmpC, AmpC-type b-lactamase; ESBL, extended-spectrum b-lactamase; KPC, Klebsiella pneumoniae carbapenemase; MDROs, multidrug-resistant organisms; N/A, not applicable; NDM, New Delhi metallo-b-lactamase; VRE, vancomycin-resistant Enterococcus spp. *Median (interquartile range). y Other: A Japanese boy aged 10 years who was admitted in India at age 6 years presented to our hospital with a chief complaint of fever of unknown origin.
ESBL (16 samples), AmpC (4 samples), and VRE (1 sample); duplications were included. Multiple MDROs were detected in 4 cases. Table 1 shows the characteristics of children with or without MDROs. MDROs were more commonly detected among children hospitalized in Eastern Asia. The distribution of the patients’ countries of previous hospitalization and rates of MDRO detection are shown in Figure 1. Klebsiella pneumoniae carbapenemase (KPC) and New Delhi metallo-b-lactamase (NDM) were identified in 3 of 23 isolates from 19 patients. All of the CPE isolates were detected from children hospitalized in China.
DISCUSSION In the present study, we uncovered 2 important findings. First, colonization by MDROs was detected in more than half of the children hospitalized abroad. Second, MDROs still rare in Japan (NDM, KPC, and VRE) were identified in some cases. A high proportion (56%) of colonization by MDROs was detected by active screening of children hospitalized abroad. In this cohort, most of the patients were from Asia, which is consistent with reports of the emerging spread of MDROs in Eastern or Southeastern Asia.4-6 The existence of underlying disease, exposure to the hospital environment, and antibiotic usage likely contributed to the high rate of colonization. A previous study from Japan reported that MDROs were found in 56.5% of adult patients previously hospitalized abroad,7 most of whom were from Asia. Recently, the prevalence of ESBL colonization was reported as 3%15% in healthy adults in Japan.8 The high proportion of colonization by MDROs in patients previously hospitalized in Asia suggests the need for preemptive infection control in countries with low MDRO prevalence.9 Genes conferring resistance to carbapenems (NDM and KPC) that are still rare in Japan were identified in 3 of 23 isolates (13.0%) of MDROs. Imipenem-resistant Pseudomonas (IMP)-type carbapenemases is prevalent nationwide in Japan, whereas carbapenemases reported from other Asian countries consist mainly of NDM and KPC.6 Such differences in the epidemiology suggest the mutual risk for all countries and potential global spread through hospitals of new CPE types that were previously absent in the community. Some reports suggest that contact precautions for MDROs do not contribute to preventing the acquisition of MDROs when compared with standard precautions.10,11 Preemptive isolation is controversial because colonization by MDROs may not result in future infection. However, we believe that preemptive infection control in our population may be valuable in preventing the spread of MDROs. Screening each patient for a history of hospitalization abroad prior to admission may provide useful information regarding infection control. In the present study, we did not perform a full investigation for potential nosocomial transmission; however, all patients with MDROs were placed on contact precautions, and no subsequent cases of colonization or infection due to NDM, KPC, or VRE were observed in this study period. There are some limitations to this study. First, the evaluation of risk factors was limited owing to the small number of cases and lack of detailed information during the hospitalization abroad, such as type and duration of antimicrobial exposure, days of hospitalization abroad, and the number and types of invasive procedures. Second, active screening was limited to rectal swab or stool samples. We did not obtain nasopharyngeal swabs to detect methicillin-resistant Staphylococcus aureus, vancomycin-intermediate S aureus, or vancomycinresistant S aureus. Third, we did not screen patients lacking a history of hospitalization abroad, and the comparison between domestic and foreign hospitalization was not performed. Further prospective studies are needed to address these issues.
ARTICLE IN PRESS K. Uda et al. / American Journal of Infection Control 00 (2019) 1−3
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Fig. 1. Rate of MDRO detection from patients hospitalized in various Asian countries. Results of active screening for children hospitalized in each country are shown. MDROs were detected in 8 out of 10 cases in China; 1 out of 2 cases in Taiwan, Philippines, and Thailand; 1 case each in Korea, Mongolia, Malaysia, Bangladesh, Nepal, and Pakistan; and no cases in Singapore, Indonesia, India, United Arab Emirates, and Uzbekistan. MDROs, multidrug-resistant organisms.
CONCLUSIONS A high proportion of colonization by MDROs was detected by active screening for children hospitalized abroad. Recognition of MDROs and preemptive infection control are needed to avoid the introduction of new modes of resistance. Acknowledgments The authors wish to thank Yoshie Sugahara and Sachiko Miura (Department of Nursing, National Center for Child Health and Development) for their efforts in infection control. The authors also thank the medical editors from the Division of Education for Clinical Research at the National Center for Child Health and Development for professionally editing this manuscript. SUPPLEMENTARY DATA Supplementary data related to this article can be found at https:// doi.org/10.1016/j.ajic.2019.08.013. References 1. Robinson TP, Bu DP, Carrique-Mas J, Fevre EM, Gilbert M, Grace D, et al. Antibiotic resistance is the quintessential one health issue. Trans R Soc Trop Med Hyg 2016;110:377-80.
2. Giske CG, Monnet DL, Cars O, Carmeli Y. Clinical and economic impact of common multidrug-resistant gram-negative bacilli. Antimicrob Agents Chemother 2008;52: 813-21. 3. Rogers BA, Aminzadeh Z, Hayashi Y, Paterson DL. Country-to-country transfer of patients and the risk of multi-resistant bacterial infection. Clin Infect Dis 2011;53: 49-56. 4. Barreto Miranda I, Ignatius R, Pfuller R, Friedrich-Janicke B, Steiner F, Paland M, et al. High carriage rate of ESBL-producing Enterobacteriaceae at presentation and follow-up among travellers with gastrointestinal complaints returning from India and Southeast Asia. J Travel Med 2016;23, tav024. 5. Karanika S, Karantanos T, Arvanitis M, Grigoras C, Mylonakis E. Fecal colonization with extended-spectrum beta-lactamase-producing Enterobacteriaceae and risk factors among healthy individuals: a systematic review and metaanalysis. Clin Infect Dis 2016;63:310-8. 6. Logan LK, Weinstein RA. The epidemiology of carbapenem-resistant Enterobacteriaceae: the impact and evolution of a global menace. J Infect Dis 2017;215(Suppl 1): 28-36. 7. Hayakawa K, Mezaki K, Sugiki Y, Nagamatsu M, Miyoshi-Akiyama T, Kirikae T, et al. High rate of multidrug-resistant organism colonization among patients hospitalized overseas highlights the need for preemptive infection control. Am J Infect Control 2016;44:e257-9. 8. Nakane K, Kawamura K, Goto K, Arakawa Y. Long-term colonization by bla(CTXM)-harboring Escherichia coli in healthy Japanese people engaged in food handling. Appl Environ Microbiol 2016;82:1818-27. 9. Islam S, Selvarangan R, Kanwar N, McHenry R, Chappell JD, Halasa N, et al. Intestinal carriage of third-generation cephalosporin-resistant and extendedspectrum beta-lactamase-producing Enterobacteriaceae in healthy US children. J Pediatric Infect Dis Soc 2018;7:234-40. 10. Harris AD, Pineles L, Belton B, Johnson JK, Shardell M, Loeb M, et al. Universal glove and gown use and acquisition of antibiotic-resistant bacteria in the ICU: a randomized trial. JAMA 2013;310:1571-80. 11. Morgan DJ, Wenzel RP, Bearman G. Contact precautions for endemic MRSA and VRE: time to retire legal mandates. JAMA 2017;318:329-30.
Contents lists available at ScienceDirect
American Journal of Infection Control journal homepage: www.ajicjournal.org
Brief Report
High proportion of multidrug-resistant organisms in children hospitalized abroad Kazuhiro Uda MD a, Takanori Funaki MD a, Kensuke Shoji MD a, Akira Kato MSc b, Isao Miyairi MD a,* a b
Division of Infectious Diseases, Department of Medical Subspecialties, National Center for Child Health and Development, Setagaya-ku, Tokyo, Japan Clinical Microbiology Laboratory, Department of Clinical Laboratory Medicine, National Center for Child Health and Development, Setagaya-ku, Tokyo, Japan
Key Words: Antibiotic-resistant bacteria Active screening Multidrug-resistant bacteria
Our infection control team initiated active screening for multidrug-resistant organisms (MDROs) among children who had been hospitalized abroad before their admission to our hospital. MDROs were detected in 19 of 34 cases (56%), including 3 isolates of Enterobacteriaceae harboring carbapenemase genes still rare in Japan. Early recognition of MDROs by screening this population may be required to avoid the introduction of new modes of resistance into the hospital environment. © 2019 Association for Professionals in Infection Control and Epidemiology, Inc. Published by Elsevier Inc. All rights reserved.
The emerging spread of multidrug-resistant organisms (MDROs) is a serious global problem.1,2 Medical tourists, expatriates, and travelers represent a source of introducing MDROs that were previously absent in the community.3 The early recognition of MDROs and preemptive infection control is important. However, the targets and tools for screening have not been established, particularly in pediatrics. In December 2014, our infection control team initiated active screening for MDROs in children who had been previously hospitalized abroad before their admission to our hospital. The aim of this study is to evaluate the proportion and characteristics of MDROs identified with active screening for children previously hospitalized abroad.
METHODS
November 2014 and December 2017. Patients’ demographic data, underlying disease, past medical history, country of previous hospitalization, and duration of hospital stay were extracted from electronic medical records. All patients admitted to our institution are required to fill out a checklist prior to hospitalization, which includes questions about history of hospitalization abroad. The preemptive infection control strategy in our institution is shown in Supplementary Figure S1. All statistical analyses were performed using IBM SPSS Statistics version 22 (IBM Corporation, Tokyo, Japan). The Fisher exact test for categorical variables and the Mann−Whitney U test for continuous variables were used for the analyses. A P value <0.05 (2sided) was considered significant. The hospital’s institutional review board approved this study (NCCHD-1793).
Study population
Screening and definition of MDROs
This observational study was conducted at the National Center for Child Health and Development in Tokyo, Japan. Our hospital is a tertiary children’s hospital with 490 beds, including a pediatric intensive care unit, a neonatal intensive care unit, and a pediatric transplant center. We included patients aged <18 years hospitalized between
We performed active surveillance only at the time of patient admission. Stool or rectal swab samples were obtained and underwent screening using blood agar and antibiotic-containing media as follows: Drigalski Agar, Modified (Becton, Dickinson and Company, Tokyo, Japan) and CHROMagar mSuper CARBA/ESBL (Kanto Chemical, Tokyo, Japan). We used an automated identification and susceptibility testing system (BD Phoenix, Becton, Dickinson and Company, Tokyo, Japan or MicroScan Walkaway, Beckman Coulter Inc, Tokyo, Japan). Antimicrobial susceptibility was determined according to the breakpoints set by the Clinical and Laboratory Standard Institute criteria [M100-S21]. Carbapenemase-producing genes were identified with the Cica Geneus Carbapenemase Genotype Detection KIT (Kanto Chemical, Tokyo, Japan). MDROs were defined as follows: AmpC-type b-lactamase (AmpC)−producing organisms,
* Address correspondence to Isao Miyairi, MD, Division of Infectious Diseases, Department of Medical Subspecialties, National Center for Child Health and Development, 2-10-1 Okura, Setagaya-ku, Tokyo 157-8535, Japan. E-mail address: [email protected] (I. Miyairi). Conflicts of interest: None to report. Author contributions: K.U. and T.F. contributed to conceptualizing the study and collected data. K.U. drafted the manuscript and performed the data analyses. K.S. and A.K. contributed to the critical revision of the manuscript. I.M. revised the manuscript and supervised the study as the corresponding author.
https://doi.org/10.1016/j.ajic.2019.08.013 0196-6553/© 2019 Association for Professionals in Infection Control and Epidemiology, Inc. Published by Elsevier Inc. All rights reserved.
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2
carbapenemase-producing Enterobacteriaceae (CPE), extendedspectrum b-lactamase (ESBL)−producing Enterobacteriaceae, and vancomycin-resistant Enterococcus (VRE) spp.
RESULTS Active screening was performed for 34 cases. The median age was 32 months (interquartile range, 15-82 months) and 23 (68%) were male patients. Previous hospitalizations in Asian countries outside of Japan were most common (29 cases, 85%), and were concentrated in Eastern Asia. Twenty-seven cases (79%) had underlying diseases, and visits for their treatment and diagnosis were the most common reason for entering our hospital. There were no patients who were evacuated or transferred directly from a foreign hospital. MDROs were detected in 19 cases (56%), including CPE (3 samples),
Table 1 Demographic data, locations of previous hospitalizations, and the microorganisms in cases with or without MDROs
Age (months)* Sex (male) Nationality Non-Japanese Underlying diseases Neurologic Gastrointestinal Liver Urologic Hematologic/Oncologic Endocrine Genetic None Reason for visit Seeking treatment Seeking diagnosis Sick during travel Immigrant Othery Location of the previous admission Asia Eastern Asia South-Eastern Asia Southern Asia Central Asia Western Asia Europe North America Central/South America Africa Duration (days) of admission in our hospital* Microorganism (including duplications) Escherichia coli (ESBL) Escherichia coli (AmpC) Escherichia coli (ESBL+AmpC) Escherichia coli (NDM) Klebsiella pneumoniae (ESBL) Klebsiella pneumoniae (NDM) Klebsiella pneumoniae (KPC) Citrobacter braakii (AmpC) Enterobacter cloacae (AmpC) Enterococcus faecium (VRE)
MDROs (+) n = 19
MDROs (−) n = 15
P Value
32 (15-82) 13 (68%)
32.5 (16-83) 10 (67%)
> .99 > .99
19 (100%) 16 (84%) 1 (5%) 1 (5%) 3 (16%) 4 (21%) 3 (16%) 4 (21%) 0 (0%) 3 (16%)
14 (93%) 11 (73%) 3 (20%) 0 (0%) 4 (24%) 0 (0%) 2 (13%) 1 (7%) 1 (7%) 4 (27%)
.44 .67 > .99 > .99 .67 .11 1.00 .35 .44 .67
6 (32%) 10 (53%) 0 (0%) 3 (16%) 0 (0%)
6 (40%) 6 (40%) 1 (7%) 1 (7%) 1 (7%)
.72 .51 .44 .61 .44
17 (89%) 11 (58%) 3 (16%) 3 (16%) 0 (0%) 0 (0%) 0 (0%) 0 (0%) 1 (5%) 1 (5%) 11 (6-30)
12 (80%) 3 (20%) 5 (33%) 2 (13%) 1 (7%) 1 (7%) 1 (7%) 2 (13%) 0 (0%) 0 (0%) 11 (8-32)
14 1 1 1 1 1 1 1 1 1
.63 — — — — — .44 .18 > .99 > .99 > .99
N/A N/A N/A N/A N/A N/A N/A N/A N/A N/A
AmpC, AmpC-type b-lactamase; ESBL, extended-spectrum b-lactamase; KPC, Klebsiella pneumoniae carbapenemase; MDROs, multidrug-resistant organisms; N/A, not applicable; NDM, New Delhi metallo-b-lactamase; VRE, vancomycin-resistant Enterococcus spp. *Median (interquartile range). y Other: A Japanese boy aged 10 years who was admitted in India at age 6 years presented to our hospital with a chief complaint of fever of unknown origin.
ESBL (16 samples), AmpC (4 samples), and VRE (1 sample); duplications were included. Multiple MDROs were detected in 4 cases. Table 1 shows the characteristics of children with or without MDROs. MDROs were more commonly detected among children hospitalized in Eastern Asia. The distribution of the patients’ countries of previous hospitalization and rates of MDRO detection are shown in Figure 1. Klebsiella pneumoniae carbapenemase (KPC) and New Delhi metallo-b-lactamase (NDM) were identified in 3 of 23 isolates from 19 patients. All of the CPE isolates were detected from children hospitalized in China.
DISCUSSION In the present study, we uncovered 2 important findings. First, colonization by MDROs was detected in more than half of the children hospitalized abroad. Second, MDROs still rare in Japan (NDM, KPC, and VRE) were identified in some cases. A high proportion (56%) of colonization by MDROs was detected by active screening of children hospitalized abroad. In this cohort, most of the patients were from Asia, which is consistent with reports of the emerging spread of MDROs in Eastern or Southeastern Asia.4-6 The existence of underlying disease, exposure to the hospital environment, and antibiotic usage likely contributed to the high rate of colonization. A previous study from Japan reported that MDROs were found in 56.5% of adult patients previously hospitalized abroad,7 most of whom were from Asia. Recently, the prevalence of ESBL colonization was reported as 3%15% in healthy adults in Japan.8 The high proportion of colonization by MDROs in patients previously hospitalized in Asia suggests the need for preemptive infection control in countries with low MDRO prevalence.9 Genes conferring resistance to carbapenems (NDM and KPC) that are still rare in Japan were identified in 3 of 23 isolates (13.0%) of MDROs. Imipenem-resistant Pseudomonas (IMP)-type carbapenemases is prevalent nationwide in Japan, whereas carbapenemases reported from other Asian countries consist mainly of NDM and KPC.6 Such differences in the epidemiology suggest the mutual risk for all countries and potential global spread through hospitals of new CPE types that were previously absent in the community. Some reports suggest that contact precautions for MDROs do not contribute to preventing the acquisition of MDROs when compared with standard precautions.10,11 Preemptive isolation is controversial because colonization by MDROs may not result in future infection. However, we believe that preemptive infection control in our population may be valuable in preventing the spread of MDROs. Screening each patient for a history of hospitalization abroad prior to admission may provide useful information regarding infection control. In the present study, we did not perform a full investigation for potential nosocomial transmission; however, all patients with MDROs were placed on contact precautions, and no subsequent cases of colonization or infection due to NDM, KPC, or VRE were observed in this study period. There are some limitations to this study. First, the evaluation of risk factors was limited owing to the small number of cases and lack of detailed information during the hospitalization abroad, such as type and duration of antimicrobial exposure, days of hospitalization abroad, and the number and types of invasive procedures. Second, active screening was limited to rectal swab or stool samples. We did not obtain nasopharyngeal swabs to detect methicillin-resistant Staphylococcus aureus, vancomycin-intermediate S aureus, or vancomycinresistant S aureus. Third, we did not screen patients lacking a history of hospitalization abroad, and the comparison between domestic and foreign hospitalization was not performed. Further prospective studies are needed to address these issues.
ARTICLE IN PRESS K. Uda et al. / American Journal of Infection Control 00 (2019) 1−3
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Fig. 1. Rate of MDRO detection from patients hospitalized in various Asian countries. Results of active screening for children hospitalized in each country are shown. MDROs were detected in 8 out of 10 cases in China; 1 out of 2 cases in Taiwan, Philippines, and Thailand; 1 case each in Korea, Mongolia, Malaysia, Bangladesh, Nepal, and Pakistan; and no cases in Singapore, Indonesia, India, United Arab Emirates, and Uzbekistan. MDROs, multidrug-resistant organisms.
CONCLUSIONS A high proportion of colonization by MDROs was detected by active screening for children hospitalized abroad. Recognition of MDROs and preemptive infection control are needed to avoid the introduction of new modes of resistance. Acknowledgments The authors wish to thank Yoshie Sugahara and Sachiko Miura (Department of Nursing, National Center for Child Health and Development) for their efforts in infection control. The authors also thank the medical editors from the Division of Education for Clinical Research at the National Center for Child Health and Development for professionally editing this manuscript. SUPPLEMENTARY DATA Supplementary data related to this article can be found at https:// doi.org/10.1016/j.ajic.2019.08.013. References 1. Robinson TP, Bu DP, Carrique-Mas J, Fevre EM, Gilbert M, Grace D, et al. Antibiotic resistance is the quintessential one health issue. Trans R Soc Trop Med Hyg 2016;110:377-80.
2. Giske CG, Monnet DL, Cars O, Carmeli Y. Clinical and economic impact of common multidrug-resistant gram-negative bacilli. Antimicrob Agents Chemother 2008;52: 813-21. 3. Rogers BA, Aminzadeh Z, Hayashi Y, Paterson DL. Country-to-country transfer of patients and the risk of multi-resistant bacterial infection. Clin Infect Dis 2011;53: 49-56. 4. Barreto Miranda I, Ignatius R, Pfuller R, Friedrich-Janicke B, Steiner F, Paland M, et al. High carriage rate of ESBL-producing Enterobacteriaceae at presentation and follow-up among travellers with gastrointestinal complaints returning from India and Southeast Asia. J Travel Med 2016;23, tav024. 5. Karanika S, Karantanos T, Arvanitis M, Grigoras C, Mylonakis E. Fecal colonization with extended-spectrum beta-lactamase-producing Enterobacteriaceae and risk factors among healthy individuals: a systematic review and metaanalysis. Clin Infect Dis 2016;63:310-8. 6. Logan LK, Weinstein RA. The epidemiology of carbapenem-resistant Enterobacteriaceae: the impact and evolution of a global menace. J Infect Dis 2017;215(Suppl 1): 28-36. 7. Hayakawa K, Mezaki K, Sugiki Y, Nagamatsu M, Miyoshi-Akiyama T, Kirikae T, et al. High rate of multidrug-resistant organism colonization among patients hospitalized overseas highlights the need for preemptive infection control. Am J Infect Control 2016;44:e257-9. 8. Nakane K, Kawamura K, Goto K, Arakawa Y. Long-term colonization by bla(CTXM)-harboring Escherichia coli in healthy Japanese people engaged in food handling. Appl Environ Microbiol 2016;82:1818-27. 9. Islam S, Selvarangan R, Kanwar N, McHenry R, Chappell JD, Halasa N, et al. Intestinal carriage of third-generation cephalosporin-resistant and extendedspectrum beta-lactamase-producing Enterobacteriaceae in healthy US children. J Pediatric Infect Dis Soc 2018;7:234-40. 10. Harris AD, Pineles L, Belton B, Johnson JK, Shardell M, Loeb M, et al. Universal glove and gown use and acquisition of antibiotic-resistant bacteria in the ICU: a randomized trial. JAMA 2013;310:1571-80. 11. Morgan DJ, Wenzel RP, Bearman G. Contact precautions for endemic MRSA and VRE: time to retire legal mandates. JAMA 2017;318:329-30.