Case Control Study Open Access
Copyright ©The Author(s) 2017. Published by Baishideng Publishing Group Inc. All rights reserved.
World J Biol Chem. Feb 26, 2017; 8(1): 95-101
Published online Feb 26, 2017. doi: 10.4331/wjbc.v8.i1.95
Device-associated infection rates, mortality, length of stay and bacterial resistance in intensive care units in Ecuador: International Nosocomial Infection Control Consortium’s findings
Estuardo Salgado Yepez, Maria M Bovera, Victor D Rosenthal, Hugo A González Flores, Leonardo Pazmiño, Francisco Valencia, Nelly Alquinga, Vanessa Ramirez, Edgar Jara, Miguel Lascano, Veronica Delgado, Cristian Cevallos, Gasdali Santacruz, Cristian Pelaéz, Celso Zaruma, Diego Barahona Pinto
Estuardo Salgado Yepez, Hugo A González Flores, Francisco Valencia, Vanessa Ramirez, Miguel Lascano, Cristian Cevallos, Cristian Pelaéz, Clínica la Merced, Quito 170401, Ecuador
Maria M Bovera, Leonardo Pazmiño, Nelly Alquinga, Edgar Jara, Veronica Delgado, Gasdali Santacruz, Celso Zaruma, Diego Barahona Pinto, Hospital de los Valles, Quito 170901, Ecuador
Victor D Rosenthal, International Nosocomial Infection Control Consortium, Buenos Aires 1429, Argentina
Author contributions: All authors were involved in study conception and design, drafting of the manuscript, provision of study patients, collection of data, critical revision of the manuscript for important intellectual content, and final approval of the manuscript; Rosenthal VD was responsible for software development, data assembly, analysis, and interpretation, epidemiologic analysis, statistical analysis and technical support.
Institutional review board statement: Every hospital’s Institutional Review Board agreed to the study protocol, and patient confidentiality was protected by codifying the recorded information, making it only identifiable to the infection control team.
Informed consent statement: All involved persons (subjects or legally authorized representative) gave their informed consent prior to study inclusion.
Conflict-of-interest statement: All authors report no conflicts of interest related to this article.
Data sharing statement: Technical appendix, statistical code, and dataset available from the corresponding author at victor_rosenthal@inicc.org.
Open-Access: This article is an open-access article which was selected by an in-house editor and fully peer-reviewed by external reviewers. It is distributed in accordance with the Creative Commons Attribution Non Commercial (CC BY-NC 4.0) license, which permits others to distribute, remix, adapt, build upon this work non-commercially, and license their derivative works on different terms, provided the original work is properly cited and the use is non-commercial. See: http://creativecommons.org/licenses/by-nc/4.0/
Correspondence to: Victor D Rosenthal, MD, Chairman, International Nosocomial Infection Control Consortium, 11 de Septiembre 4567, Floor 12, Apt 1201, Buenos Aires 1429, Argentina. victor_rosenthal@inicc.org
Telephone: +54-11-47047227
Received: September 17, 2016
Peer-review started: September 19, 2016
First decision: November 14, 2016
Revised: December 31, 2016
Accepted: January 16, 2017
Article in press: January 18, 2017
Published online: February 26, 2017

Abstract
AIM

To report the results of the International Nosocomial Infection Control Consortium (INICC) study conducted in Quito, Ecuador.

METHODS

A device-associated healthcare-acquired infection (DA-HAI) prospective surveillance study conducted from October 2013 to January 2015 in 2 adult intensive care units (ICUs) from 2 hospitals using the United States Centers for Disease Control/National Healthcare Safety Network (CDC/NHSN) definitions and INICC methods.

RESULTS

We followed 776 ICU patients for 4818 bed-days. The central line-associated bloodstream infection (CLABSI) rate was 6.5 per 1000 central line (CL)-days, the ventilator-associated pneumonia (VAP) rate was 44.3 per 1000 mechanical ventilator (MV)-days, and the catheter-associated urinary tract infection (CAUTI) rate was 5.7 per 1000 urinary catheter (UC)-days. CLABSI and CAUTI rates in our ICUs were similar to INICC rates [4.9 (CLABSI) and 5.3 (CAUTI)] and higher than NHSN rates [0.8 (CLABSI) and 1.3 (CAUTI)] - although device use ratios for CL and UC were higher than INICC and CDC/NSHN’s ratios. By contrast, despite the VAP rate was higher than INICC (16.5) and NHSN’s rates (1.1), MV DUR was lower in our ICUs. Resistance of A. baumannii to imipenem and meropenem was 75.0%, and of Pseudomonas aeruginosa to ciprofloxacin and piperacillin-tazobactam was higher than 72.7%, all them higher than CDC/NHSN rates. Excess length of stay was 7.4 d for patients with CLABSI, 4.8 for patients with VAP and 9.2 for patients CAUTI. Excess crude mortality in ICUs was 30.9% for CLABSI, 14.5% for VAP and 17.6% for CAUTI.

CONCLUSION

DA-HAI rates in our ICUs from Ecuador are higher than United States CDC/NSHN rates and similar to INICC international rates.

Key Words: Ventilator-associated pneumonia, Catheter-associated urinary tract infection, Healthcare-associated infection, Antibiotic resistance, Developing countries, Intensive care unit, Surveillance, Central line-associated bloodstream infections, Hospital infection

Core tip: This is a prospective, cohort, surveillance study on device-associated infection rates, mortality, length of stay and bacterial resistance conducted in intensive care units (ICUs) in Ecuador from October 2013 to January 2015. Device-associated healthcare-acquired infection rates in our ICUs from Ecuador are significantly higher than United States Centers for Disease Control and Prevention’s National Healthcare Safety Network’s rates and similar to International Nosocomial Infection Control Consortium’s international rates.


  • Citation: Salgado Yepez E, Bovera MM, Rosenthal VD, González Flores HA, Pazmiño L, Valencia F, Alquinga N, Ramirez V, Jara E, Lascano M, Delgado V, Cevallos C, Santacruz G, Pelaéz C, Zaruma C, Barahona Pinto D. Device-associated infection rates, mortality, length of stay and bacterial resistance in intensive care units in Ecuador: International Nosocomial Infection Control Consortium’s findings. World J Biol Chem 2017; 8(1): 95-101
  • URL: https://www.wjgnet.com/1949-8454/full/v8/i1/95.htm
  • DOI: https://dx.doi.org/10.4331/wjbc.v8.i1.95

INTRODUCTION

Device-associated healthcare-acquired infections (DA-HAIs) are one of the main threats to the safety of patients, causing patient morbidity, mortality, excess costs and prolonged length of hospital stay (LOS), particularly in intensive care settings of limited-resource countries[1-3].

Multifaceted infection prevention programs integrating target DA-HAI surveillance methods were proved effective in several United States studies, which showed the occurrence of DA-HAI could be reduced by more than 30%, along with an analogous reduction in DA-HAI-related hospital costs[4].

Antimicrobial-resistant infections is another primary issue that needs to be addressed in infection control programs in order to prevent the spread of resistant strains through the report of DA-HAI-associated pathogens and their susceptibility to antibiotics[5].

During the last four decades, the United States Centers for Disease Control and Prevention (CDC)’s National Healthcare Safety Network (NHSN)[6] has developed benchmarking data on DA-HAIs in intensive care unit (ICU) patients, which has afforded the International Nosocomial Infection Control Consortium (INICC) an essential insight[5].

The INICC is an open, international, non-profit, collaborative healthcare-associated infection (HAI) control network comprised of 2000 hospitals in 500 different cities in 66 countries in Africa, Asia, Eastern Europe, Latin America and the Middle East transcontinental region[5,7]. Since it was established in 1998 in Argentina, it has been the first multi centre surveillance and research network centered on the reduction of the rates of DA-HAI in the ICU and of hospital-wide surgical site infections through tools and resources provided for free to healthcare centers to assist them in with the prevention and control this public health burden through the implementation of infection prevention programs[6-9]. The INICC network operates by means of an online surveillance system - the INICC Surveillance Online System (ISOS) - and a systematic multidimensional approach - the INICC Multidimensional Approach (IMA) - whose effectiveness for the decrease of DA-HAI rates was shown in the scientific literature[8-23]. The ISOS applies the definitions of HAIs developed by the CDC/NHSN and standardized methodologies, thereby promoting applied research and evidence-based infection prevention practices.

This is the first study to report an analysis of data on DA-HAI rates from Ecuador using ISOS between October 2013 and January 2015 in 2 ICUs from 2 hospitals of the INICC network[5].

MATERIALS AND METHODS
Background on INICC

The INICC is focused on the surveillance and prevention of HAI in adult, pediatric ICUs and neonatal ICUs, step down units, inpatient wards, and of surgical site infections in surgical procedures hospital wide[5]. Through the ISOS, INICC provides free training and surveillance tools to hospitals worldwide, which allows them to measure HAI consequences, and to evaluate the impact of infection control and prevention practices[24].

Study design and setting

This is a prospective surveillance, cohort study made on all the patients admitted, between October 2013 and January 2015, to 2 adult medical/surgical ICUs from 2 medium-sized hospitals (1 private and 1 public hospital) in Quito, Ecuador, through the implementation of the IMA. The IMA uses 6 components for HAI control to be applied simultaneously, as follows: (1) bundles of infection control interventions; (2) educational and training sessions; (3) outcome surveillance on HAI-related rates; (4) process surveillance; (5) feedback on HAI rates and their related adverse effects; and (6) feedback on health care workers’ performance[5].

In accordance with the INICC protocol, hospitals’ identities are kept under confidentiality and patient data was anonymized. Due to the fact that this was an epidemiological surveillance study, which did not include tests of experimental drugs, biomedical devices or products, and that patient data were anonymized, an informed consent was not necessary according to the ethics committees that evaluated and approved the study.

ISOS

The ISOS applied CDC/NSHN’s methods and definitions published in January 2015[25], and also included INICC methodology. The methods developed by the CDC/NSHN to determine HAI rates indicate that the numerators are the total number of each type of HAIs, and the denominators are the device days recorded from all ICU patients, in the form of pooled data; that is, the number of device days and the characteristics of a particular patient are not calculated[25]. By contrast, the INICC methodology, through the implementation of the ISOS, included the collection of data per specific patient, from all ICU patients (with and without HAI), including surrogates of HAI (low blood pressure, high temperature, antibiotic therapy, results of cultures, LOS and mortality), and data on risk factors, including invasive devices. To have data on all ICU patients enabled a match of patients with and without HAI by various patient features necessary to calculate excess mortality, LOS and HAI-related hospital cost[5].

Analysis and collection of data

Infection control professionals (ICPs) uploaded their daily-collected data on DA-HAIs using ISOS. Data on central line-associated bloodstream infection (CLABSI), ventilator-associated pneumonia (VAP), and catheter-associated urinary tract infection (CAUTI), denominator data, patient-days and specific device-days in the ICUs were used to determine the rates of each DA-HAI per 1000 device days, LOS and mortality, as follows: (1) device days equaled the number of central line (CL)-days, mechanical ventilator (MV)-days and urinary catheter (UC)-days; (2) DA-HAI crude excess mortality equaled crude mortality of patients with DA-HAI hospitalized in the ICU minus crude mortality of ICU patients who had not acquired a DA-HAI; (3) DA-HAI crude excess LOS equaled crude LOS of patients with DA-HAI hospitalized in the ICU minus crude LOS of patients ICU patients who had not acquired a DA-HAI; and (4) Device utilization ratio (DUR) equaled the number of device days divided by the number of bed days[5].

Training

ICPs were trained at hospitals by the INICC team. Instruction manuals, training tools and tutorial movies describing in detail how to conduct surveillance and upload data to ISOS were also provided to ICPs. Finally, ICPs received technical and methodological support from the INICC team via email, telephone calls and webinars.

Definitions

The ISOS applied the definitions and criteria published in 2015 by CDC’s NHSN for HAI surveillance[25].

Statistical analysis

Data analysis and the calculation of rates of DA-HAI, LOS, mortality, device utilization were done using ISOS version 2.0 (City of Buenos Aires, Argentina). Relative risk ratios, P-values and 95% confidence intervals were calculated using SPSS 16.0 (SPSS Inc. an IBM company, Chicago, Illinois, United States) and EpiInfo® version 6.04b (CDC, Atlanta, GA, United States). The statistical review of the study was done by a biomedical statistician.

RESULTS

From October 1st 2013 to January 30th 2015, 776 patients were admitted to the 2 participating medical/surgical ICUs, for a total of 4818 bed days. During the study period, the mean length of participation of each ICU was as follows: + SD 14.5 + 2.1 mo, range from 13 to 16 mo.

Table 1 provides data on crude excess LOS and mortality in all patients (with and without DA-HAI) admitted to the ICUs over the period of study. CLABSI was associated with the highest pooled excess mortality in the ICUs. The excess LOS of patients with CAUTI was the greatest among the analyzed DA-HAIs.

Table 1 Pooled means of the distribution of crude mortality, crude excess mortality, length of stay, and crude excess length of stay, of adult intensive care unit patients with and without device-associated healthcare-acquired infection.
PatientsPatients, nDeaths, nPooled crude mortality, %Pooled crude excess mortality, % (95%CI)LOS, total daysPooled average, LOS (d)Pooled average, excess LOS (d) (95%CI)
Without DA-HAI67810715.80-35795.3
With CLABSI15746.7030.9 (8.1-54.7)19012.77.4 (5.8-9.2)
With CAUTI12433.3017.6 (-3.2-46.4)17414.59.2 (7.3-11.4)
With VAP431330.2014.5 (4.1-27.4)43410.14.8 (4.1-5.7)

Table 2 shows the DA-HAI rates and related results of this report from Ecuador benchmarked against the INICC report of data from 43 countries for the period 2007-2012, against the United States CDC/NHSN report of 2013 and against the United States NHSN report of 2009-2010[6,26,27].

Table 2 Benchmarking of device-associated healthcare-acquired infection rates, device utilization and antimicrobial resistance in this report against the report of the International Nosocomial Infection Control Consortium (2007-2012) and the reports of the United States Centers for Disease Control and Prevention’s National Healthcare Safety Network data (2013 and 2009-2010).
This reportINICC report (2007-2012)[26]United States CDC/NHSN report (2013)[6]/2009-2010[27]
95%CI95%CI
Medical/surgical ICU
Central line, DUR1.24 (1.21-1.27)0.54 (0.54-0.54)0.37
CLABSI rate6.5 (4.6-8.9)4.9 (4.8-5.1)0.8
Mechanical ventilator, DUR0.32 (0.31-0.34)0.36 (0.36-0.36)0.24
VAP rate44.3 (34.4-56.0)16.5 (16.1-16.8)1.1
Urinary catheter, DUR0.77 (0.74-0.79)0.62 (0.62-0.62)0.54
CAUTI rate5.7 (3.5-8.7)5.3 (5.2-5.8)1.3
Antimicrobial resistance % (n)
Pathogen, antimicrobialCLABSI (n)CLABSICLABSI
Staphylococcus aureus
Oxacillin60% (5)61.20%54.60%
Pseudomonas aeruginosa
Ciprofloxacin71.4% (7)37.50%30.50%
Piperacillin or piperacillin-tazobactam100% (5)33.50%17.40%
Amikacin71.4% (7)42.80%10.00%
Imipenem or meropenem71.4% (7)42.40%26.10%
Klebsiella pneumoniae
Ceftriaxone or ceftazidime60% (5)71.20%28.80%
Imipenem or meropenem20% (5)19.60%12.80%
Acinetobacter baumanii
Imipenem or meropenem100% (2)66.30%62.60%

DA-HAI rates pooled means were as follows: 6.5 (n, 39) CLASBIs per 1000 CL-days, with a DUR of 1.24 for 5998 CL-days; 44.3 (n, 69) VAPs per 1000 MV-days, with a DUR of 0.32 for 1559 MV-days, and 5.7 (n, 21) CAUTIs per 1000 UC-days, with a DUR of 0.77 for 3699 UC-days.

Overall, our CLABSI and CAUTI rates were similar to the INICC report data, but our VAP rate was substantially higher than INICC’s. On the other hand, the incidence rates of DA-HAI were higher compared with United States NHSN report data. Our DURs for CL and UC were higher compared both to United States NHSN’s and INICC’s; however, our DUR for MV was lower than INICC’s. Most of the resistance rates found in our ICUs were significantly higher than those found in the US ICUs as reported by the CDC’s NHSN.

DISCUSSION

DA-HAIs in Ecuador have not been systematically analyzed in the scientific literature to date. The incidence of DA-HAIs in this study is significantly higher than other recent analogous studies carried out in Latin America. In Colombia, it was recently shown that DA-HAI rates per 1000 device days were higher than ours: The CLABSI rate was 47.4, the VAP rate was 32.3, and the CAUTI rate was 20.3[28]. By contrast, pooled crude mortality was higher in our study than in a study conducted in Colombia, whose findings showed the crude unadjusted mortality attributable to DA-HAI was 18.5% for patients with CLABSI (95%CI: 1.42-2.87); 16.9% for patients with VAP (95%CI: 1.24-3.00); and 10.5% for patients with CAUTI (95%CI: 0.78-3.18)[28]. In Peru, Cuellar et al[29] found a CAUTI rate of 5.1 per 1000 UC days, a VAP rate of 31.3 per 1000 MV days and a CLABSI rate of 7.7 per 1000 CL-days. In a comparable study conducted in Brazil, Salomao et al[30] found a rate of 20.9 VAPs per 1000 MV days, a CAUTI rate of 9.6 per 1000 UC days and a CLABSI rate of 9.1 per 1000 CL days.

The statistically significantly higher rates of DA-HAI rates and DURs found in the analyzed ICUs of Ecuador compared with the rates reported by the US CDC’s NHSN represent the current burden of HAIs in high-income countries[6]. On the other hand, CLAB and CAUTI rates found in the international INICC Report (2007-2012) for 43 countries[26], which would represent middle and low-income economies, were similar to our rates, although our pooled DURs were higher for CL and UC[6,26]. By contrast, although our VAP rate was remarkably higher than INICC’s, our DUR for MV was lower, which means there are other risk factors different from DURs influencing DA-HAI rates. Regarding antimicrobial resistance, the resistance percentages found in this study were also higher than those found in United States CDC’s NHSN[27] and INICC[26] reports’ for Pseudomonas aeruginosa as resistant to piperacillin-tazobactam, ciprofloxacin, amikacin, and imipenem or meropenem, as well as the resistance percentages determined for Acinetobacter baumanii to imipenem or meropenem.

Different factors can elucidate the possible reasons for these higher DA-HAI rates compared with the United States CDC’s NHSN and INICC’s reports. As also occurs in other developing countries, we consider that adherence to infection control bundles in Ecuador is variable, there is frequently a low nurse-patient staffing ratio (with a nurse-patient ratio higher than 4:1) and the number of experienced nurses or trained healthcare workers is deficient - which has been demonstrated as significantly associated with considerably high DA-HAI incidence rates in the ICU patient[31]. In addition, there is hospital over-crowding. According to World Health Organization standards[32], there should be between 8 and 10 hospital beds available per 1000 persons, but in 2011, in Ecuador, there were only 1.5 per 1000, with many hospitals remaining at full capacity[33].

The risk of infection of patients hospitalized in ICUs can be reduced though the implementation of surveillance targeted on DA-HAI, because it is successful to focus on characteristics of the burden of DA-HAIs. These surveillance data is necessary to increase ICPS’s sensitivity and aids them to detecting HAIs and avoiding underreporting[5].

In addition, surveillance should be complemented with the performance of other practices for DA-HAI control and prevention[34,35]. Therefore, INICC has played a crucial by facilitating free infection prevention tools and resources through the use of ISOS, as well as by fostering increasing awareness about the risks posed by DA-HAIs amongst health care professionals[5,36].

Limitations

The difference in time periods for the diverse data sources was not considered for the benchmarking of our findings against the United States CDC’s NSHN and INICC reports. Due to the low economic resources of our ICUs, very few cultures were taken, which could have influenced the rates of CLABSI and CAUTI, as they could not be document because they did not fulfill all the United States CDC/NHSN criteria. In addition, the number of patients to whom blood and/or urine cultures should have been taken, but were actually not due to lack of economic resources, is unknown as this data was not registered.

Conclusions

The findings of this study highlight that DA-HAIs pose major challenges for public health and the wellbeing of patients in Ecuador. One of INICC’s primary goals is to provide health care facilities worldwide with free tools and resources to support the introduction of systematic infection prevention practices in order to address this burden effectively by accomplishing a reduction in DA-HAI rates and their adverse effects.

ACKNOWLEDGMENTS

The authors thank the many healthcare professionals at each member hospital who assisted with the conduct of surveillance in their hospital; Mariano Vilar and Débora López Burgardt, who work at INICC headquarters in Buenos Aires; the INICC Country Directors and Secretaries (Haifaa Hassan Al-Mousa, Hail Alabdaley, Areej Alshehri, Altaf Ahmed, Carlos A Álvarez-Moreno, Anucha Apisarnthanarak, Bijie Hu, Hakan Leblebicioglu, Yatin Mehta, Toshihiro Mitsuda, and Lul Raka); and the INICC Advisory Board (Carla J Alvarado, Nicholas Graves, William R Jarvis, Patricia Lynch, Dennis Maki, Toshihiro Mitsuda, Cat Murphy, Russell N Olmsted, Didier Pittet, William Rutala, Syed Sattar, and Wing Hong Seto), who have so generously supported this unique international infection control network.

COMMENTS
Background

The International Nosocomial Infection Control Consortium (INICC) program is focused on surveillance of device-associated healthcare-acquired infections (DA-HAIs) in the intensive care units (ICUs), step down units and general wards, and surveillance of SSIs hospital wide. This particular study was focused on ICUs, because they are the healthcare settings that represent the highest HAI rates, due to patients’ critical condition and exposure to invasive devices. Through the last 12 years, INICC has undertaken a global effort in Africa, Eastern Mediterranean, Europe, Latin America, South East Asia and Western Pacific to prevent and control DA-HAIs, and has achieved extremely successful results, by increasing hand hygiene compliance, improving compliance with other infection control bundles and interventions as described in several INICC publications, and consequently reducing the rates of DA-HAI and mortality. To compare a hospital's DA-HAI rates with the rates identified in this report, it is required that the hospital team concerned collect their data by applying the methods and methodology described for United States NHSN and INICC, and then calculate infection rates and DU ratios for the DA-HAI Module.

Applications

The particular and primary application of these data is to serve as a guide for the implementation of prevention strategies and other quality improvement efforts in Ecuador for the reduction of DA-HAI rates to the minimum possible level.

Peer-review

This is a nice prospective multi-center trial showing similar nosocomial infection rates in Ecuadorian hospitals as compared with international hospitals.

Footnotes

Manuscript source: Invited manuscript

Specialty type: Biochemistry and molecular biology

Country of origin: Argentina

Peer-review report classification

Grade A (Excellent): A, A

Grade B (Very good): 0

Grade C (Good): C

Grade D (Fair): 0

Grade E (Poor): 0

P- Reviewer: Gonzalez-Reimers E, Gupta VK, Rodricks MB S- Editor: Ji FF L- Editor: A E- Editor: Li D

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13.  Leblebicioglu H, Yalcin AN, Rosenthal VD, Koksal I, Sirmatel F, Unal S, Turgut H, Ozdemir D, Ersoz G, Uzun C. Effectiveness of a multidimensional approach for prevention of ventilator-associated pneumonia in 11 adult intensive care units from 10 cities of Turkey: findings of the International Nosocomial Infection Control Consortium (INICC). Infection. 2013;41:447-456.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 29]  [Cited by in F6Publishing: 28]  [Article Influence: 3.6]  [Reference Citation Analysis (0)]
14.  Mehta Y, Jaggi N, Rosenthal VD, Rodrigues C, Todi SK, Saini N, Udwadia FE, Karlekar A, Kothari V, Myatra SN. Effectiveness of a multidimensional approach for prevention of ventilator-associated pneumonia in 21 adult intensive-care units from 10 cities in India: findings of the International Nosocomial Infection Control Consortium (INICC). Epidemiol Infect. 2013;141:2483-2491.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 26]  [Cited by in F6Publishing: 10]  [Article Influence: 3.3]  [Reference Citation Analysis (0)]
15.  Rosenthal VD, Álvarez-Moreno C, Villamil-Gómez W, Singh S, Ramachandran B, Navoa-Ng JA, Dueñas L, Yalcin AN, Ersoz G, Menco A. Effectiveness of a multidimensional approach to reduce ventilator-associated pneumonia in pediatric intensive care units of 5 developing countries: International Nosocomial Infection Control Consortium findings. Am J Infect Control. 2012;40:497-501.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 51]  [Cited by in F6Publishing: 48]  [Article Influence: 5.1]  [Reference Citation Analysis (0)]
16.  Rosenthal VD, Rodríguez-Calderón ME, Rodríguez-Ferrer M, Singhal T, Pawar M, Sobreyra-Oropeza M, Barkat A, Atencio-Espinoza T, Berba R, Navoa-Ng JA. Findings of the International Nosocomial Infection Control Consortium (INICC), Part II: Impact of a multidimensional strategy to reduce ventilator-associated pneumonia in neonatal intensive care units in 10 developing countries. Infect Control Hosp Epidemiol. 2012;33:704-710.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 65]  [Cited by in F6Publishing: 58]  [Article Influence: 7.2]  [Reference Citation Analysis (0)]
17.  Rosenthal VD, Ramachandran B, Villamil-Gómez W, Armas-Ruiz A, Navoa-Ng JA, Matta-Cortés L, Pawar M, Nevzat-Yalcin A, Rodríguez-Ferrer M, Yıldızdaş RD. Impact of a multidimensional infection control strategy on central line-associated bloodstream infection rates in pediatric intensive care units of five developing countries: findings of the International Nosocomial Infection Control Consortium (INICC). Infection. 2012;40:415-423.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 60]  [Cited by in F6Publishing: 57]  [Article Influence: 6.7]  [Reference Citation Analysis (0)]
18.  Rosenthal VD, Guzman S, Pezzotto SM, Crnich CJ. Effect of an infection control program using education and performance feedback on rates of intravascular device-associated bloodstream infections in intensive care units in Argentina. Am J Infect Control. 2003;31:405-409.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 119]  [Cited by in F6Publishing: 106]  [Article Influence: 7.0]  [Reference Citation Analysis (0)]
19.  Higuera F, Rosenthal VD, Duarte P, Ruiz J, Franco G, Safdar N. The effect of process control on the incidence of central venous catheter-associated bloodstream infections and mortality in intensive care units in Mexico. Crit Care Med. 2005;33:2022-2027.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 100]  [Cited by in F6Publishing: 23]  [Article Influence: 6.3]  [Reference Citation Analysis (0)]
20.  Jaggi N, Rodrigues C, Rosenthal VD, Todi SK, Shah S, Saini N, Dwivedy A, Udwadia FE, Mehta P, Chakravarthy M. Impact of an international nosocomial infection control consortium multidimensional approach on central line-associated bloodstream infection rates in adult intensive care units in eight cities in India. Int J Infect Dis. 2013;17:e1218-e1224.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 48]  [Cited by in F6Publishing: 47]  [Article Influence: 6.0]  [Reference Citation Analysis (0)]
21.  Leblebicioglu H, Öztürk R, Rosenthal VD, Akan ÖA, Sirmatel F, Ozdemir D, Uzun C, Turgut H, Ersoz G, Koksal I, Özgültekin A, Esen S, Ulger F, Dilek A, Yilmaz H, Dikmen Y, Aygún G, Tulunay M, Oral M, Ünal N, Cengiz M, Yilmaz L, Geyik MF, Şahin A, Erdogan S, Sacar S, Sungurtekin H, Uğurcan D, Kaya A, Kuyucu N, Yýlmaz G, Kaya S, Ulusoy H, İnan A. Impact of a multidimensional infection control approach on central line-associated bloodstream infections rates in adult intensive care units of 8 cities of Turkey: findings of the International Nosocomial Infection Control Consortium (INICC). Ann Clin Microbiol Antimicrob. 2013;12:10.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 40]  [Cited by in F6Publishing: 39]  [Article Influence: 5.0]  [Reference Citation Analysis (0)]
22.  Rosenthal VD, Guzman S, Safdar N. Effect of education and performance feedback on rates of catheter-associated urinary tract infection in intensive care units in Argentina. Infect Control Hosp Epidemiol. 2004;25:47-50.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 76]  [Cited by in F6Publishing: 66]  [Article Influence: 4.5]  [Reference Citation Analysis (0)]
23.  Leblebicioglu H, Ersoz G, Rosenthal VD, Yalcin AN, Akan OA, Sirmatel F, Turgut H, Ozdemir D, Alp E, Uzun C. Impact of a multidimensional infection control approach on catheter-associated urinary tract infection rates in adult intensive care units in 10 cities of Turkey: International Nosocomial Infection Control Consortium findings (INICC). Am J Infect Control. 2013;41:885-891.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 41]  [Cited by in F6Publishing: 31]  [Article Influence: 5.1]  [Reference Citation Analysis (0)]
24.  Kanj SS, Zahreddine N, Rosenthal VD, Alamuddin L, Kanafani Z, Molaeb B. Impact of a multidimensional infection control approach on catheter-associated urinary tract infection rates in an adult intensive care unit in Lebanon: International Nosocomial Infection Control Consortium (INICC) findings. Int J Infect Dis. 2013;17:e686-e690.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 21]  [Cited by in F6Publishing: 15]  [Article Influence: 2.6]  [Reference Citation Analysis (0)]
25.  Navoa-Ng JA, Berba R, Rosenthal VD, Villanueva VD, Tolentino MC, Genuino GA, Consunji RJ, Mantaring JB. Impact of an International Nosocomial Infection Control Consortium multidimensional approach on catheter-associated urinary tract infections in adult intensive care units in the Philippines: International Nosocomial Infection Control Consortium (INICC) findings. J Infect Public Health. 2013;6:389-399.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 19]  [Cited by in F6Publishing: 13]  [Article Influence: 2.4]  [Reference Citation Analysis (0)]
26.  Rosenthal VD, Maki DG, Mehta Y, Leblebicioglu H, Memish ZA, Al-Mousa HH, Balkhy H, Hu B, Alvarez-Moreno C, Medeiros EA. International Nosocomial Infection Control Consortium (INICC) report, data summary of 43 countries for 2007-2012. Device-associated module. Am J Infect Control. 2014;42:942-956.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 146]  [Cited by in F6Publishing: 128]  [Article Influence: 24.3]  [Reference Citation Analysis (0)]
27.  Sievert DM, Ricks P, Edwards JR, Schneider A, Patel J, Srinivasan A, Kallen A, Limbago B, Fridkin S. Antimicrobial-resistant pathogens associated with healthcare-associated infections: summary of data reported to the National Healthcare Safety Network at the Centers for Disease Control and Prevention, 2009-2010. Infect Control Hosp Epidemiol. 2013;34:1-14.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 1004]  [Cited by in F6Publishing: 890]  [Article Influence: 111.6]  [Reference Citation Analysis (0)]
28.  Moreno CA, Rosenthal VD, Olarte N, Gomez WV, Sussmann O, Agudelo JG, Rojas C, Osorio L, Linares C, Valderrama A. Device-associated infection rate and mortality in intensive care units of 9 Colombian hospitals: findings of the International Nosocomial Infection Control Consortium. Infect Control Hosp Epidemiol. 2006;27:349-356.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 69]  [Cited by in F6Publishing: 69]  [Article Influence: 4.6]  [Reference Citation Analysis (0)]
29.  Cuellar LE, Fernandez-Maldonado E, Rosenthal VD, Castaneda-Sabogal A, Rosales R, Mayorga-Espichan MJ, Camacho-Cosavalente LA, Castillo-Bravo LI. Device-associated infection rates and mortality in intensive care units of Peruvian hospitals: findings of the International Nosocomial Infection Control Consortium. Rev Panam Salud Publica. 2008;24:16-24.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 45]  [Cited by in F6Publishing: 12]  [Article Influence: 3.5]  [Reference Citation Analysis (0)]
30.  Salomao R, Rosenthal VD, Grimberg G, Nouer S, Blecher S, Buchner-Ferreira S, Vianna R, Maretti-da-Silva MA. Device-associated infection rates in intensive care units of Brazilian hospitals: findings of the International Nosocomial Infection Control Consortium. Rev Panam Salud Publica. 2008;24:195-202.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 42]  [Cited by in F6Publishing: 11]  [Article Influence: 3.5]  [Reference Citation Analysis (0)]
31.  Rosenthal VD, Maki DG, Salomao R, Moreno CA, Mehta Y, Higuera F, Cuellar LE, Arikan OA, Abouqal R, Leblebicioglu H. Device-associated nosocomial infections in 55 intensive care units of 8 developing countries. Ann Intern Med. 2006;145:582-591.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 292]  [Cited by in F6Publishing: 257]  [Article Influence: 19.5]  [Reference Citation Analysis (0)]
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35.  Rosenthal VD, Maki DG, Rodrigues C, Alvarez-Moreno C, Leblebicioglu H, Sobreyra-Oropeza M, Berba R, Madani N, Medeiros EA, Cuéllar LE. Impact of International Nosocomial Infection Control Consortium (INICC) strategy on central line-associated bloodstream infection rates in the intensive care units of 15 developing countries. Infect Control Hosp Epidemiol. 2010;31:1264-1272.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 103]  [Cited by in F6Publishing: 98]  [Article Influence: 9.4]  [Reference Citation Analysis (0)]
36.  Rosenthal VD, Al-Abdely HM, El-Kholy AA, AlKhawaja SA, Leblebicioglu H, Mehta Y, Rai V, Hung NV, Kanj SS, Salama MF. International Nosocomial Infection Control Consortium report, data summary of 50 countries for 2010-2015: Device-associated module. Am J Infect Control. 2016;44:1495-1504.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 144]  [Cited by in F6Publishing: 137]  [Article Influence: 28.8]  [Reference Citation Analysis (0)]